A Mnemonic Theory of Odor Perception

Richard J . Stevenson
MacquarieUniversity
Robert A. Boakes
University of Sydney
Thepsychological basisof odor qualityispoorlyunderstood. For pragmaticreasons, descriptionsof odor
quality generally rely onprofilingodors interms of what odorants they bringto mind. It is arguedhere
that this reliance on profiling reflects a basic property of odor perception, namely that odor quality
depends on theimplicit memories that an odorant elicits. This is supportedby evidenceindicatingthat
odor quality as well as ones ability to discriminate odors is affected by experience. Developmental
studies and cross-cultural research also point to this conclusion. In this article, these findings are
reviewed and amodel that attempts to account for themis proposed. Finally, themodels consistency
with both neurophysiological and neuropsychological datais examined.
Progressinunderstandingtheperceptionof stimulusqualitiesin
vision and audition has been based on the search for systematic
relationships betweenthephysical attributes of astimulus andthe
subjectiveexperienceit produces; that is, on solvingthestimulus
problem. Recent developments in molecular biology and neuro-
physiology haveresultedinconsiderableadvances inresearchers
knowledge of the olfactory receptor system, which has hitherto
laggedwell behindtheknowledgeof other sensory systems. Nev-
ertheless, asdetailedbelow, major problemsremainfor anytheory
of odor quality based solely on the physical properties of the
stimulus. A solutionof thestimulusproblemfor olfactionappears
to remain remote. A different approach to the analysis of odor
qualities is onethat takes into account theeffects of past experi-
ence on the way that an individual perceives an odor. In this
article, we review recent experimental evidence on such effects
and present a theory of odor perception that is based on the
assumption that the qualities perceived in an odor reflect the
normally implicit memoriesthat it elicits. Althoughthesubjective
experienceinducedbyanodor clearlyconsistsof morethanjustits
perceptual qualities (e.g., its hedonic ones), intheabsenceof any
extant psychological theoriesof olfaction, modelsof basicpercep-
tual processes are likely to be more useful. Consequently, our
primary focus hereremains perceptual.
TheHuman Olfactory System
The olfactory systemis characterized by having two discrete
modes of stimulation (Chifala& Polzella, 1995, Figure1; Rozin,
1982). Chemical stimuli canbetransportedtotheolfactory recep-
torsviathenosethroughsniffing(orthonasal perception) or viathe
release of volatile chemicals in the mouth during eating and
drinking(Pierce& Halpern, 1996). Thesevolatilesthenascendvia
the posterior nares of the nasopharynx to stimulate the olfactory
receptors (retronasal perception). Although there are some rela-
tively minor differences between the two modes of stimulation,
mainly resultingfromtheless efficient flowof air duringretrona-
sal perception, crucially both result in binding to thesameset of
receptors (Burdach & Doty, 1987; Voirol & Daget, 1986).
It is useful to draw a distinction between taste and smell,
becausetheseterms arecommonly confused. Tasteis ananatom-
ically discretesensefromsmell andischaracterizedby four types
of sensation (sweet, sour, salty, and bitter [and possibly a fifth,
umami]), whicharedetectedby receptors or ionchannels located
primarily onthetongue(McLaughlin& Margolskee, 1994). Most
basictastantslikesodiumchloride, sucrose, quinine, andcitricacid
have no smell, just as many odor stimuli completely lack taste.
This is typically confirmed by placing asubstanceon thetongue
while the nose is firmly pinched to prevent retronasal olfaction.
Any sensation is then most likely to betaste.
A further distinctionis betweentheolfactory andnasal trigem-
inal systems. The nasal trigeminal systemis mediated separately
fromthesenseof smell andreferstoreceptorslocatedinthenasal
passageandinall parts of thesystemthat comeinto contact with
inhaled substances. These receptors have at least two effects on
olfaction (seeGreen & Lawless, 1991). First, thesensations they
evoke, such as burning, itching, and stinging, areexperienced as
part of the spectrum of olfactory sensations (Laska, Distel, &
Hudson, 1997). Second, trigeminal irritationappearstoreducethe
perceived intensity of pure odors (Cain & Murphy, 1980). This
articleis primarily concerned with olfactory stimulation.
The main function of the olfactory receptors is to transduce
chemical stimuli intopatternsof neural activitythat, after process-
ing, allowthestimulustobediscriminatedfromthousandsof other
odorous stimuli (Hildebrand & Shepherd, 1997). The olfactory
receptorsarelocatedontheolfactorymucosa(seeFigure1), which
is arranged in two discrete segments; one of these is accessed
exclusively fromtheleft nostril, and theother is accessed exclu-
sively fromthe right (Lanza & Clerico, 1995). Each segment is
Richard J . Stevenson, Department of Psychology, Macquarie Univer-
sity, New South Wales, Australia; Robert A. Boakes, Department of
Psychology, University of Sydney, Sydney, Australia.
WethankDavidLaing, J udi Homewood, FredWestbrook, Trevor Case,
J udi Wilson, andJ ulieFitness for their many helpful comments onearlier
versions of this article.
Correspondenceconcerningthis articleshouldbeaddressedto Richard
J . Stevenson, Department of Psychology, Macquarie University, New
South Wales 2109, Australia. E-mail: rstevens@psy.mq.edu.au
Psychological Review Copyright 2003 by theAmerican Psychological Association, Inc.
2003, Vol. 110, No. 2, 340364 0033-295X/03/$12.00 DOI: 10.1037/0033-295X.110.2.340
340
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covered with a layer of mucus that is vital for normal function
(Pelosi, 1996). The mucus probably assists chemical stimuli to
diffuse onto the olfactory receptor neurons, as well as removing
stimuli after transduction. The receptor neurons project into the
mucus, andthereceptorsarelocatedontheir cilia(for review, see
Buck, 1996, 2000; Hildebrand & Shepherd, 1997).
Olfactory receptorshavebeenidentifiedasbelongingtoalarge
familyof biologicallyactivemoleculescalledG-proteins (Buck &
Axel, 1991). Although this and many related discoveries, dis-
cussedbelow, havebeenmadeusingmiceandrats, thesefindings
almost certainly apply to other mammals and to humans (Issel-
Tarver & Rine, 1997; Mombaerts, 1999). TheG-proteinreceptors
are embedded in the cell membrane of the cilia, and when an
effectivechemical stimulus arrives thebindingresults indepolar-
ization and an action potential (Hildebrand & Shepherd, 1997).
Only certaintypes of chemical appear to beeffectivestimuli, that
is, stimuli detectableby theolfactory system. First, they must fall
within a certain range of solubility. Methane, for example, is
relatively insoluble in water and odorless but can be smelled by
divers as solubility increases with higher air pressure (Laffort &
Gortan, 1987). Volatility, and hence molecular size, is a further
limitation, with few chemicals being odorous if they exceed a
molecular weight of around 300 (Ohloff, Winter, & Fehr, 1991).
The way that chemical stimuli might interact with olfactory
receptors has generated alargenumber of theories. Thesecan be
groupedinto threegeneral classes: chemical (e.g., Amoore, 1964;
Boelens, 1974; Henning, 1916; Laska, Trolp, & Teubner, 1999),
vibrational (e.g., Dyson, 1938; Turin, 1996; Wright, 1977), and
enzymatic (which is not discussed further here; see Amoore,
1982). Two of these, chemical and vibrational, havereceived the
most attention. Chemical theories can be further subdivided into
thosebasedonthephysiochemical propertiesof thestimulus, such
asitsoverall shapeor thepresenceof particular functional groups
(which is themorepopular view) or on themolecules reactivity
(which has received far less support). Both chemical theory sub-
typespresumethat odorsbindtoparticular receptor typesandthat
the pattern of activity fromthese different receptors generates a
representation of thestimulus that is complex and unique(Beets,
1978; Schiffman, 1974; Sullivan, Ressler, & Buck, 1995).
Vibrational theories also come in two forms. The first, now
largely discredited, assumes that chemicals emit particular fre-
quenciesthat aredetectedbythereceptorsinthesamewaythat the
visual system senses light (see Moncrieff, 1951). More recent
forms of vibrational theory start fromthepremisethat molecules
haveparticular setsof vibrational frequenciesthat uniquely define
them (Turin, 1996; Wright, 1977). These theories propose that
olfactory receptors are tuned to detect different vibrational fre-
quencies andthereforearepresentationof thestimulus is built up
fromthis uniquepattern of vibrations.
It is currently estimatedthat theadult humanolfactory mucosa
containsbetween500and750uniqueG-proteinreceptors(Buck&
Axel, 1991). Thisfindingalonesetsolfactionapart fromtheother
senses, each of which contain only a limited number of receptor
types. Eacholfactoryreceptor neuronappearstoproduceonlyone
typeof G-proteinreceptor (Malnic, Hirono, Sato, & Buck, 1999),
andit isimportant tonotethat eachreceptor typeappearssensitive
to many different chemicals (Malnic et al., 1999; Mombaerts,
1999). Familiesof particular G-proteinreceptor typesappear tobe
locatedtogether ontheolfactory epithelium(Ressler, Sullivan, &
Buck, 1993), although the location of individual receptor types
within such areas appears random. Thefunctional significanceof
this arrangement is not understood.
Followinganinteractionbetweenachemical andtheG-protein
receptor, thecell depolarizes, andanactionpotential passesalong
to the first stage of information processing, the glomeruli, con-
tained in the olfactory bulb (Sullivan & Dryer, 1996). There are
estimatedtobebetween1,000and2,000glomeruli. Eachglomer-
ulusreceivesinput primarilyfromasingleG-proteinreceptor type
(Ressler, Sullivan, & Buck, 1993). The apparent mismatch be-
tweennumber of glomeruli andnumber of receptor types reflects
acurrent lack of precision in measurement; thegeneral natureof
this relationshipis all that is of concerninthis article. Thespatial
arrangement of glomeruli appears to be the same as that for
receptorsontheolfactoryepithelium, inthat membersof thesame
G-protein families tend to be located close together (see Mori,
Nagao, & Yoshihara, 1999). One possible consequence of this
arrangement is that chemical stimuli that resemble each other in
whatever key feature(s) turn out to be important for receptor
binding will also tend to activate neighboring glomeruli. As in
other sensorysystems, lateral inhibitionoccursbetweenglomeruli.
Thus, high activation of oneglomerulus may suppress activity in
its neighbors andthus sharpenoutput tothenext processingstage
(Yokoi, Mori, & Nakanishi, 1995; but see Laurent, 1999, for an
alternativeperspective).
A key implication to emerge from this account is that odor
quality is very unlikely to bedictatedby one-to-onerelationships
between particular receptors and an associated quality. This is
becauseof thesheer multitudeof receptors, their apparent lack of
specificity, the fact that most odorous stimuli are composed of
manychemicals, andthegeneral observationthat olfactorycoding
isprobablyrepresentedattheneural level byacomplexspatial and
temporal pattern of activity at the glomeruli that is relatively
unique to every chemical stimulus (e.g., Buck, 1996, 2000;
Figure 1. Cross-sectionof thehead, illustratingthedual natureof olfac-
tory stimulation (via the nose or nasal pharynx) and the separateness of
taste(tongue) andsmell (olfactory mucosa). FromSensation and Percep-
tion (5thed., p. 451), by E. B. Goldstein, Copyright 1999. Reprintedwith
permissionof Brooks/Cole, animprint of theWadsworthGroup, adivision
of Thomson Learning.
341
A MNEMONIC THEORY OF ODOR PERCEPTION
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Haberly, 1998; Malnic et al., 1999; Rubin& Katz, 1999; Sullivan
et al., 1995).
This perspective, which has emerged mainly from molecular
biology and neurophysiology over the last decade, has received
little if any attention from experimental psychologists, and the
implications for psychological accounts of odor quality have re-
mainedlargely unexplored. Infact, as wediscuss below, psycho-
logical researchonodor-quality perceptionhasbeenmotivatedby
thestimulus-problemapproach, in which onereceptor is equated
with onequality. In light of recent physiological findings it may
comeas no surprisethat thesedataprovidelittlesupport for this
way of thinking.
Odor Quality and theStimulus Problem
Thepsychological study of odor quality beganwithself-reports
of olfactory experience, later coupled with an attempt to identify
commonsensory categories across different chemical stimuli (see
Amoore, 1982). This effort stemmed from the hope that such
categorizationwouldleadtothediscovery of alimitednumber of
primaryodor sensations. It wasthenthought that theidentification
of correspondingreceptor typesandtheunravelingof thestimulus
problemwould follow, just as it had for color perception (Saha-
kian, 1981). In this section wediscuss various approaches to the
description of olfactory qualities, starting with a brief historical
background.
Linnaeus(seeAmoore, 1982) wasthefirst toattempt asystem-
atic classification of olfactory sensation. He categorized plant
odors into seven categories, in an effort largely motivated by his
studiesof plant taxonomy rather thanof olfactory perception. The
first general classification systemwas proposed by Rimmel (see
Moncrieff, 1951) and included 18 categories, with a bias toward
categorizationbasedonvegetativeorigin. A moreabstract system
was proposedby Zwaardemaker (seeMoncrieff, 1951). This con-
tained 9 main categories, each of which was further divided into
two or threesubcategories.
Modern attempts to identify odor primaries begin with Hen-
nings (1916) odor prism. Each corner of the prismrepresents a
primaryquality, thesebeing, flowery, foul, fruity, spicy, burnt, and
resinous. Henning claimed that odors would either be fully cap-
turedbyaprincipal descriptor or fall onthesurfaceor edgesof the
prismif intermediate between categories. This claimproduced a
flurry of experimental work that was largely unsupportive. The
general problemwasthesameasmet by all classificationsystems
(Moncrieff, 1951): Manyodorscouldnotbeaccommodatedwithin
theschemeor, as inthis case, locatedonthesurfaceof theprism
(e.g., Findley, 1924; Hazzard, 1930; MacDonald, 1922). For ex-
ample, inMacdonalds (1922) study, geraniol was judgedto have
threeprincipal qualities, thesebeingflowery, fruity, andresinous,
yet theconstructionof theprismimplies that this odor must have
afurther quality, spiciness. Participants judgments werenot con-
sistent with this prediction.
More recent attempts at defining primary odor qualities have
also met with problems. Amoore(1952) identified terms used by
chemists to describeodors. Thesewerethen analyzed to identify
thosemost commonlyused. Seventermswereidentified: ethereal,
camphor, minty, floral, musky, putrid, and burnt. Amoore and
Venstrom(1967) foundsignificant correlationsbetweentheterms
characterizing particular chemicals and their molecular shape,
suggesting seven or so primary qualities and hence receptors.
However, Amoores other approach, theidentification of specific
anosmiasanalogous to the study of anomalous color vision
revealed amuch larger number of specific anosmias (about 43 at
last count; Amoore, 1982), andthisfindingisdifficult toreconcile
withtheearlier conclusionof sevenprimaries. Overall, attemptsto
identify odor primaries must bejudged as unsuccessful.
A second approach to the analysis of odor quality has arisen
fromthe needs of professionals (e.g., sensory evaluation panels,
expert tasters, perfumers, flavorists, and wine tasters) for a stan-
dardizeddescriptivesystemthat captures thedifferences between
odors and promotes communication between specialists (e.g.,
Brud, 1986). Inonesuchsystematarget odor is comparedwitha
setof standardodors, withparticipantsratingthetargetssimilarity
to each comparison stimulus (e.g., Brud, 1986; Schultz, 1964).
However, this approach has proved unwieldy and has seen little
general application. Much more popular have been systems in
which a target odor is evaluated in relation to a standard list of
verbal descriptors (e.g., Dravnieks, 1985; Noble et al., 1987).
Harper, Bate-Smith, andLand(1968) pioneeredthefirst systemof
this kind by collecting a large number of terms used to describe
odor quality. Thesewerethenwinnoweddowntoaset of 44items,
against which participants evaluate the target odor. Dravnieks
(1985) later extended thenumber of items in his widely used list
to 146. Thereis, however, no strict limit on thenumber of items
that couldbeincluded, apart fromobviouspractical considerations
likeparticipant fatigue. Thesesystemsallowanodor tobeprofiled
quiterapidly, withparticipantsratingeachdescriptor ondegreeof
presence(effectivelyasimilarityrating). Theprofiledevelopedfor
aparticular odor using this techniqueshows high testretest reli-
ability (Dravnieks, 1982).
Threepoints about descriptiveprofilingarepertinent here. The
first is that most of these schemes either explicitly or implicitly
involvesimilarity judgments, in that theparticipant is effectively
askedto assess howsimilar thetarget is to aparticular descriptor
(Lawless, 1999). Thispoint isillustratedbytheobviousprediction
that odors that receive similar profiles should also be judged,
globally, as more similar. Precisely such a relationship has been
observed(Dravnieks, Bock, Powers, Tibbetts, & Ford, 1978). The
secondpoint concernstheitemstowhichtheodor iscompared. In
thevast majority of cases theseitems arespecific odorous objects
or categories of objects (Lawless, 1999). Third, and most impor-
tant of all, each of these rating schemes appears to need a large
number of descriptors tocaptureadequately, if indeedit does, the
experienceof odor quality. This wouldseemto suggest that there
areno primary odor qualities (for asimilar conclusion seeChas-
trette, Elmouaffek, & Sauvegrain, 1988).
Applying Adaptation and Discrimination
to theStimulus Problem
An alternative approach to the stimulus problemhas been to
study olfactory adaptation and discrimination. We turn first to
adaptation, whichis asalient property of odor perception(Engen,
1982). Repeated or prolonged exposure produces a marked de-
creaseintheperceivedintensityof anodor, asmeasuredbyarange
of psychophysical techniques (Koster, 1971). This propensity can
beusedtostudythestimulusprobleminthefollowingway. If two
odorssmell similar, it isareasonablepresumptionthat they might
342
STEVENSON AND BOAKES
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also share the same receptor types. It follows that taking two
odorants that smell similar andpresentingoneof themrepeatedly
might produce cross-adaptation when the other similar smelling
odor is sniffed (e.g., Cain & Polak, 1992).
The results fromsuch cross-adaptation studies are equivocal.
Althoughsomeodor pairsthat arequalitatively similar will cross-
adapt (see, e.g., Cain & Polak, 1992; Pierce, Wysocki, Aronov,
Webb, & Boden, 1996), others will not (Todrank, Wysocki, &
Beauchamp, 1991). Moreover, many odors that are clearly dis-
criminableandhavevery different qualities will cross-adapt (Ko-
ster, 1971). Inaddition, odors that arestructurally similar andyet
perceptually distinct may also show cross-adaptation (Pierce,
Zeng, Aronov, Preti, & Wysocki, 1995), and in some cases pre-
exposuretotheadaptingodor may evenact toincreasethejudged
intensity of the test stimulus (Engen & Bosak, 1969). These
findingsargueagainst theideaof any simplerelationshipbetween
perceptual similarity and commonality of receptor types.
Theuseof discriminationtoexploreodor qualityisbasedonthe
assumption that theeaseof discriminating two odors is inversely
relatedtothedegreethat theyshareperceptual qualities(e.g., J ehl,
Royet, & Holley, 1994). Fromthis perspective, odors that sharea
commonstructural feature(if this shouldbeimportant incausing
odor quality) should beless discriminablethan odors that do not
sharethis feature. Studies using odor discrimination arenot only
themost objective(Wise, Olsson, & Cain, 2000) but alsotheleast
explored. This is probably becauseof thepractical costs imposed
by themany comparisontrialsneededtoobtainsufficient datafor
meaningful analysis andby theproblemthat adaptationprecludes
theshort intertrial intervals that canbeusedinequivalent studies
of vision or audition.
The effect of chemical structure on discriminability has been
examined in a number of recent studies using both primate and
human participants. The chemical structure of an odorant, most
notably itscarbonchainlengthanditsfunctional groups, hasbeen
foundtoaffect discriminabilityinalawful way, suchthat odorants
of greater structural similarity are generally less distinguishable
(Laska, Ayabe-Kanamura, Hubener, & Saito, 2000; Laska &
Teubner, 1999; Laska et al., 1999). These results suggest that
various aspects of a chemicals structure undoubtedly influence
participants perception of odor quality. However, there is also
evidence to suggest that such relationships are far fromperfect
(e.g., Boelens, 1974; Polak, 1973).
TheRoleof Learning in Odor-Quality Perception
Theguidingprincipleof psychological inquiryintoodor quality
isbasedonthepresumptionthatsensationresultscausallyfromthe
features of the stimulus and that with sufficient searching these
featuresandtheir sensationswill beidentified, solvingthestimulus
problem. Withinsuchaframework, perceptionof anodor should
not be greatly influenced by past experience. However, recent
researchontheroleof learninginodor perceptionchallenges this
assumption and suggests that perception of an odor is far more
sensitive to past experience than is the case for other modalities
(for asimilar conclusionbasedontheanimal literature, seeHud-
son, 1999).
One phenomenon that clearly makes this point is tastesmell
synesthesia, whereby olfactory stimulation can give rise to an
experiencethat properly belongs to thesensory modality of taste.
It has been known for sometimethat participants will spontane-
ously describe a wide range of odors as smelling sweet; notable
examples are strawberry, vanilla, and caramel (Harper et al.,
1968). It isnot clear whythistermisused, becausesweet normally
refers toasensationproducedby stimulationof tastereceptors on
thetongueandnothingcorrespondingtoanolfactorysweet recep-
tor is known to exist. One possibility is that describing odors in
terms of sweetness, or other tasteterms, is alinguistic phenome-
nonwithsweet usedinametaphorical rather thaninaperceptual
way. However, the sweetness-enhancement effect argues against
thispossibility. For example, if participantsareaskedtojudgethe
sweetness of asucrosesolution flavored by strawberry, they will
judgethemixturetobesweeter thantheunflavoredsucrose(Frank
& Byram, 1988; Frank, Ducheny, & Mize, 1989). Thesizeof this
effect isdirectly relatedtohowsweet theodor smells(Stevenson,
Prescott, & Boakes, 1999). This suggests that the perceptual ex-
perience of sweetness produced by something in the mouth is
based on a combination of sensory signals fromthemouth, gen-
eratedby(a) odorlesssweettastantssuchassucroseand(b) signals
producedby retronasal stimulationof olfactory receptorsby taste-
lessodorants. Sweetnessenhancement isnot theonlyeffect of this
kind. Sweet odors used to flavor a sour solution can reduce the
perceived sourness of the latter, whereas nonsweet odors can
reducetheperceivedsweetnessof asucrosesolution(Stevensonet
al., 1999). In addition, the sweet taste of saccharin, but not the
meaty taste of monosodium glutamate, can facilitate threshold
detectionof thesweet smellingodor benzaldehyde, apparently via
their shared quality of sweetness (Dalton, Doolittle, Nagata, &
Breslin, 2000).
Many sweet-smelling odors have a history of co-occurrence
with sweet tastes. This has led to the suggestion that the odor
quality sweet may be acquired on the basis of individual experi-
ence (Frank & Byram, 1988; and see Laska et al., 1997, for a
relatedsuggestionfor sour) and, further, that it maybemodifiable
by varying the co-occurrence of odors and tastes in a laboratory
setting. We have repeatedly obtained such an effect, odortaste
learning, over a series of experiments (Stevenson, Boakes, &
Prescott, 1998; Stevenson, Boakes, & Wilson, 2000a, 2000b;
Stevenson, Prescott, & Boakes, 1995). These have all used the
samebasic procedure. Participantsrateaset of odorsonanumber
of dimensionsintwoidentical sniffingtests, apre- andaposttest.
In theintervening training phasethey areasked to tastethat is,
sip, swirl aroundthemouth, andthenexpectorateaseriesof fluid
samples. Some samples consist of a sucrose solution to which a
target odor has beenaddedas aflavorant andothers may contain
a citric acid solution, tasting moderately sour, or plain water
flavored by adding further target odors. In general wehaveused
target odors that participants find only vaguely familiar and nor-
mally cannot identify. Lychee and water chestnut have been the
targets usedinmost of theseexperiments. Thesniffingtests have
usually requiredlinear analogratingsonfour scales: liking, inten-
sity, sweetness, and sourness.
Such experiments have consistently produced the same result.
Target odors that have been mixed with sucrose are rated as
sweeter, andlesssour, intheposttest thantheywereinthepretest,
whereas thosemixed with citric acid arerated as less sweet, and
moresour, at posttest. Thereis littlechangefrompre- to posttest
in theratings for control odors mixed with water during training,
other than aslight increasein intensity (Stevenson et al., 1998).
343
A MNEMONIC THEORY OF ODOR PERCEPTION
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Becausesuch adesign raises thepotential problemof demand
characteristics, the initial experiments contained conditions de-
signedtoobscuretheir purpose. Theseincludedtheinclusioninthe
training phase of an irrelevant taska triangle test requiring
participants to decidewhich of threesamples was different from
theother twoandof moredummythancritical trials, withspaced
training over several sessions. Recognition tests to assess aware-
ness and postexperiment questionnaires revealed that participants
had no understanding of the purpose of the experiment and very
little, if any, explicit memoryof whichflavor hadbeenmixedwith
which taste. Learning of odortastecontingencies appeared to be
implicit, inthat thesizeof thelearningeffect wasunrelatedtothe
degreeof awareness of thecontingencies shown by a participant
(Stevenson et al., 1998, 1995). Later experiments suggested that
elaboratemaskingproceduresareunnecessary. Theeffect wasalso
obtainedwhendummytrialswereremovedandtrainingcompleted
in a single session, yet participants still displayed little explicit
memoryfor theodortastecontingencies(Stevensonet al., 2000a).
The size of the effect, produced by between four and eight
pairings of an odor with sucrose, is an increase of sweetness of
about 10 points on a 100-point scale under the range of experi-
mental conditionsusedtodate. Thiseffectsizedoesnotseemtobe
affected by whether the solutions are sampled froma cup in the
manner describedaboveor sippedthroughastraw(i.e., precluding
serial learning of smell then taste). It is also very stable. When
retested1monthafter training, nodetectablechangewasfoundin
participants ratings(Stevensonet al., 1998). Anunexpectedfind-
ingwas that theeffect is resistant to bothextinctionandcounter-
conditioning. In these experiments an odor was first mixed with
citric acid and then for 12 trials presented in water (Stevenson et
al., 2000a) or in sucrose solution (Stevenson et al., 2000b). No
difference was detected in the posttest ratings between an odor
given this extinction or counter-conditioning treatment and one
givenodorsournesspairingsalone. Bothodorsshowedodortaste
learning relative to control odors. In contrast, colortaste associ-
ations proved sensitive to both the extinction and the counter-
conditioningprocedures. Oneexperimental manipulationthat can
decrease odortaste learning is to provide preexposure to an
odorby presenting it as a flavorant mixed in waterprior to
addingit toasucroseor citric acidsolution(Stevenson& Boakes,
inpress). Thesignificanceof thesevariouspropertiesof odortaste
learning are discussed further below, but first we consider other
experiential treatments that change the way that an odor is
perceived.
Oneof theseinvolves what wetermodor-quality exchange or
odorodor learning. Exposuretoacombinationof odors, A X,
canimbueA withsomeof Xsperceptual qualities, andviceversa.
Experimentsexaminingthiseffect havecontainedatrainingphase
inwhichparticipantssniff twosuchcombinations, A X andB
Y. Each combination of atarget odor (A, B) with acontaminant
(X, Y) is presented 12 times over two separate sessions. This is
followed by aposttest in which A, B, X, and Y arepresented on
their ownandparticipants areaskedto rateeachof theminterms
of howA-like, B-like, X-like, andY-liketheysmell. For example,
X couldbep-anisaldehyde, whichisgenerally perceivedassmell-
ingmusty, andinthiscaseX-like wouldmeanratingeachodor for
mustiness. Acquisitionof thisodor qualityisthenmeasuredbythe
difference between musty ratings for Target A and the same
ratings for Control Odor B, which has not been mixed with
p-anisaldehyde. With such a design, odor pairings are varied
across groups in counterbalanced fashion.
Experiments usingtheseprocedures haveexaminedacquisition
of odor properties using a number of targets (L-carvone, with a
minty smell; cis-3-hexanol, green or fresh grass; terpineol, disin-
fectant-like; methyl salicylate, mint or peppermint; guaiacol,
smoky; champignol, mushroom; and wood distillate, woody or
resinous) and various contaminants, including water chestnut
(fruity), p-anisaldehyde (musty), cherry (cherry or berry), and
citral (lemony). Exposureto aparticular target-contaminant mix-
turedoes not always produceachangeintheperceivedquality of
thetarget. For example, neither L-carvonenor cis-3-hexanol were
detectably more fruity after being mixed with water chestnut.
Furthermore, on some occasions the effect occurs in only one
direction: Anodor canyieldsomepropertywithout acquiringany,
and vice versa. Thus, in the same study (Stevenson, 2001a)
L-carvone was rated more musty after being mixed with
p-anisaldehyde, but thelatter wasnot ratedasmoreminty. It isnot
yet possibleto predict whether acontaminant will affect atarget
odor. One important factor appears to be the detectability of the
components within the mixture (Stevenson, 2001b). Another re-
latedissueisthefamiliarity or nameability of thecomponents; for
example, wooddistillatewasthemost easilyidentifiedtarget odor
and also theoneleast modified by acontaminant in Stevensons
(2001b) study.
Theaboveresultsarebasedonratingsfromsmall setsof scales.
This raises thepossibility that theoutcomes may begreatly influ-
enced by the particular labels given to the scales (e.g., Clark &
Lawless, 1994). Further measures takenintheaboveexperiments
suggest that thisisunlikely. All four experimentsof thiskindhave
included a second posttest in which participants have rated the
similarity of pairs of odors. This was to test the prediction that
followingexposuretoamixtureof Target A withContaminant X,
A should berated as moresimilar to X than to Control Odor Y.
Such an effect was found but, in general, only for pairs in which
the first posttest revealed transfer of odor qualities (Stevenson,
2001a, 2001b). A further test, includedinoneexperiment (Steven-
son, 2001b), required participants to rate each odor on the 146
attributes used by Dravnieks (1985). Although less sensitive a
testpossibly because given lastthis measure revealed effects
of training similar to those detected by the limited number of
scales of thefirst posttest.
Learning and Odor Discrimination
To this point, theevidencewehavereviewed on theeffects of
learning on odor perception has relied on ratings of subjective
experience. Suchmeasureshavetheir limitations, notably because
of differences across individuals in the way that scale labels are
interpreted (Wise et al., 2000) and wider concerns with the reli-
ability of self-report data. Thus, it is clearly important toexamine
theextent towhichobjectivemeasuresof odor perception, notably
discrimination performance, areaffected by past experience.
At least twofactors havebeenidentifiedthat canimproveodor
discriminability: mereexposureandlabel learning. Several exper-
iments have demonstrated enhanced discrimination following
mereexposureto aset of odors. Rabin(1988; Experiment 1) had
agroup of participants profileaset of seven odors of lowfamil-
iarityandnear neutral hedonictoneusingtheDravnieks(1985) set
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STEVENSON AND BOAKES
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of scales. In the subsequent samedifferent discrimination test
their performanceequivalent toabout 88%correctwassignif-
icantly better than that of the two nonexposed control groups at
81% correct. Enhancement of performance in such tests of odor
discrimination can be obtained following prior exposure even
when no task is required of participants. J ehl, Royet, and Holley
(1995) gave different groups 0, 1, 2, or 3 exposures to sets of
odors, asking participants to sniff each odor for 4 s and remain
silent. A subsequent samedifferent test revealedthat discrimina-
tionperformanceincreasedwithprior exposure, mainly reflecting
decreased false-alarmrates, with a d of about 4.0 for the group
given threeexposures and d of about 1.6for thegroup given no
preexposure.
Although the previous two experiments demonstrate that dis-
crimination improves with experience, they potentially confound
perceptual and memorial processes because of their reliance on
comparison between two temporally discrete stimuli. A further
experiment by Rabin (1988, Experiment 2) argues against this
possibility, because he obtained largely similar results to those
above under conditions in which the task involved simultaneous
presentation of two stimuli in amixture. In this caseparticipants
weregivenatarget (e.g., A) followed(or preceded) onsometrials
bythetarget mixedwithacontaminant (e.g., A X). Participants
thenjudgedsameor different as inRabins (1988) Experiment 1.
He found that prior familiarity with both target and contaminant
produced a considerable improvement in discrimination, with
scores equivalent to 58% correct when neither was familiar to
about 87%whenbothwerefamiliar. Whyexposureshouldbenefit
bothsuccessiveandsimultaneous discriminationtasks is not well
understood, andno adequatetheoretical explanationcurrently ex-
ists for any of theseeffects.
Learninglabels for aset of odors canfurther improvediscrim-
inability beyond the effect of mere exposure (which one should
note is a necessary condition for label learning to occur). Rabin
(1988, Experiment 1) had another group of participants label the
sameseven odors that wereprofiled by theexposuregroup. The
label group subsequently performed significantly better than the
exposure group on the samedifferent task (94% correct, com-
paredwith88%intheexposuregroupand81%inthenonexposed
control groups). Although the precise nature of the benefit con-
ferredby label learningis unknown, at least two possibilities can
be canvassed. On most discrimination tests, as noted above, a
delayispresentbetweenthepresentation(or theperception) of one
stimulusandthepresentation(or theperception) of thesubsequent
comparison stimulus. Labels may provide an easy verbal short-
hand, allowingtheodorsidentitytobestoredinworkingmemory
(e.g., seeAnnett & Leslie, 1996, for theadverseeffects of verbal
suppression on an odor-memory task). A second, less prosaic
explanation can also be made, on the basis of the notion that
languageshapesperception. Thisperspectivehasbeenmorecom-
monlyadoptedwhenconsideringindividualswhohavesomeform
of special olfactory expertise (e.g., perfumers or wine experts).
Expertise in such individuals is usually characterized by both
perceptual knowledge and an extensive related vocabulary (e.g.,
see Solomon, 1990). Wine expertsthe most tested groupare
undoubtedly better at wine discrimination than nonexperts (e.g.,
Hughson& Boakes, 2001; Lawless, 1984). However, thesebene-
fits tend to be small when appropriate exposure controls are
present (individuals with large amounts of perceptual experience
but no specialized vocabulary; see Melcher & Schooler, 1996).
Whether this linguistic benefit shown by experts represents a
difference in perceptual experience or simply a better ability to
describeandremember odorsinverbal form(assuggestedearlier)
is yet to beresolved.
Although label learning and mere exposure may typically en-
hancediscriminability, exposurecan in certain circumstances re-
duce it. Experimental research with both humans and animals
usingstimuli other thanodorshasshownthat whentwocueshave
producedacommonoutcomethey canbecomeless discriminable
(e.g., Honey& Hall, 1989; Katz, 1963). FollowingJ amess(1890)
study, thishasbeenreferredtoasacquired equivalence incontrast
with acquired distinctiveness (Hall, 1991). The previous section
referred to evidence fromexperiments on the exchange of odor
qualities indicatingthat after two odors havebeenexperiencedas
a mixture they are judged as more similar (Stevenson, 2001a,
2001b). Because similarity judgments should to some extent be
predictiveof discriminability, thisfindingsuggeststhat experienc-
ing two odors together might make later discrimination between
them more difficult. Following the training procedures in our
previous experiments (A X, B Y), we conducted triangle
tests, whichrevealedpoorer discriminationbetweenelementspre-
viously mixed together (A vs. X, B vs. Y; mean correct trials
77%) thanbetweenunmixedpairs(A vs. Y, B vs. X; meancorrect
trials 87%; Stevenson, 2001c). More recent experiments, in
whichonly oneodor mixtureis experienced(i.e., A X or B
Y) followed by triangle tests involving comparisons of both A
versus X and B versus Y have revealed that the elements of the
preexposed mixturearemoredifficult to tell apart (mean correct
trials 77%) thannon-preexposedstimuli (meancorrect trials
89%; Stevenson&Case, inpress). Thus, thisprocessappearstobe
oneof acquired equivalence.
Cross-Cultural Differences in Odor Perception
Theresearch reviewed in theprevious two sections has shown
that the way people experience and discriminate between odors
can be significantly affected by relatively brief experiences in a
laboratory setting. This suggests that differences in odor percep-
tionacrossculturescouldbequitelarge. Culturesdiffer intheir use
of dietary flavorings andstaples (Moore, 1970), their exposureto
culturally specific odors (e.g., church incense), and also in their
use of odorants in different contexts (e.g., cleaning agents, per-
fumes, medicinal flavors).
Unfortunately for our purposes, most cross-cultural researchon
odorshasfocusedonaffectiveresponses(Pangborn, 1975; Rozin,
1978). There appears to be only one published study, Ayabe-
Kanamura et al. (1998), and a conferenceabstract, Ueno (1993),
that have reported data on the qualities that participants from
different cultures perceive when smelling the same odorant. In
Ayabe-Kanamura et al.s (1998) study, German and J apanese
participantswereaskedtosmell arangeof culturallyspecific(e.g.,
aniseed for Germans, dried fish for J apanese) and international
odors(e.g., coffee). J udgmentsof likingrevealed, asexpected, that
culturally specific odors were more preferred by their respective
groups. Moreimportant herearedifferencesbetweenparticipants
reports about the qualities of many of the odors. Many German
participantsthoughtthatfermentedsoyabeanswerereminiscentof
cheesy smelly feet, that driedfishsmelledof excrement, and
345
A MNEMONIC THEORY OF ODOR PERCEPTION
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soy sauceof fresh bread, but fewJ apanesethought so (Ayabe-
Kanamuraet al., 1998, p. 34). Conversely, aniseedwas evaluated
as disinfectant-like and Indian ink as medicinal by J apanese
participantsbut quitedifferentlybyGermans(Ayabe-Kanamuraet
al., 1998, p. 34).
Uenos(1993) study comparedJ apaneseandSherpa(Nepalese)
participants perceptions of 20J apanesefoodflavors. Inthis case
participantswereaskedtoarrangethebottlescontainingtheodors
into groups on the basis of their similarity. Cluster analysis re-
vealed that fishy odors were characterized in a different way by
Sherpaparticipants, in that they did not exist as adistinct cluster
as they didfor theJ apanese. Fishodors arerarely encounteredby
Sherpas in their nativeNepal.
Apart fromsupporting theclaimthat differences in experience
can produce alterations in odor quality, Uenos study also indi-
cated a close positive relationship between quality and liking.
Where odors differed markedly in quality between groups (e.g.,
driedfish), theyalsotendedtodiffer markedlyinpleasantness. On
the basis of this finding, the much larger literature relevant to
cross-cultural effects on liking is also consistent with theconclu-
sionthatexperienceaffectstheperceivedqualityof anodor aswell
as howmuchit is liked(e.g., Davis & Pangborn, 1985; Schaal et
al., 1997; Wysocki, Pierce, & Gilbert, 1991).
A Mnemonic Theory of Odor Perception
We noted at the start of this article that psychological ap-
proaches to odor-quality perceptionhavebeendrivenby attempts
tosolvethestimulusproblem, withvisual or auditorypsychophys-
icsasanimplicit model. However, it hasnowbeenrecognizedthat
understanding visual and auditory perception, particularly object
recognition (Logothetis & Sheinberg, 1996) and auditory scene
analysis (Bregman, 1990), requires much morethan simply solv-
ing the stimulus problem. In fact Bregman (1990) argued that
undue emphasis on such a purely psychophysical approach has
probably retarded understanding of auditory perception. Herewe
argue that an understanding of odor quality cannot be achieved
without full reference to how we process olfactory information,
becauseodor-quality perceptionbears amuchcloser resemblance
to activities such as sceneanalysis and object recognition than it
does to psychophysical studies using single frequencies of light
and puretones. This is becauseno such equivalent is possiblein
olfaction, becauseall olfactory stimuli result incomplex temporal
and spatial patterns of activation on the glomerular layer (e.g.,
Laurent, 1999). The emphasis for a psychological level explana-
tion of odor-quality perception must be the way in which this
patternof activationisdealt with. Thisformsthecentral part of the
theory that weadvancein this section.
The mnemonic theory is described first in information-
processing terms fromtheperspectiveof its corefunction (odor-
quality perception; seeFigure2) andthenfromtheperspectiveof
its implications for related functions (e.g., familiarity, learning,
priming, memory, imagery). A commentary ontheseassumptions
follows. We then discuss whether the proposed system can be
mappedontodifferent parts of thecentral nervous systemandthe
extent to which the theory provides a better understanding of
abnormalities of odor perceptionfollowingvarious kinds of dam-
ageto thebrain.
Overview
Theessenceof themnemonic theory isthat thecomplex output
patternfromtheglomeruli forms themodels input (Number 1on
Figure2). Thisinput isthencomparedinparallel withthecontents
of astorecomposedprimarily of previously encounteredglomer-
ular patterns (Number 2aon Figure2). Thegreater thesimilarity
betweenthecurrent input patternandastoredpattern(anengram),
the greater the activation of that engram. Odor quality is repre-
sented hereas therelativeactivation of theseengrams.
Assumption 1 (Tabula Rasa)
Odors, in themain, do not possess any inherent psychological
properties beyond their degree of presence (intensity). For the
newborn human infant most odorants producenothing morethan
a blooming, buzzing confusion, to borrow J amess (1890, p.
488) phrase. This is in contrast with tastants, which possess both
sensory and hedonic psychological properties that areunambigu-
ously innate. Although this assumption is provocative, evidence
does favor this account, as wemakeclear later.
Assumption 2 (Input Pattern)
Any stimulus falling within the bounds of detectability (e.g.,
molecular weight), will produceacomplex anduniquepattern of
Figure 2. Diagrammatic representation of themnemonic theory of odor
perception.
346
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stimulation, both spatial and temporal, across theglomeruli. This
will occur irrespective of the stimuluss molecular simplicity or
complexityor thenumber of itschemical components. Thispattern
forms both the input for the theory (Number 1 on Figure 2) and
provides thebasis for theperception of odor intensity.
Assumption 3 (What Is the Pattern Compared With?)
Thecoreelementof thetheoryisaprocessingmodule(olfactory
processingmodule; seeFigure2), inwhichtheinput is compared
in parallel with all previous encodingsengrams (Number 2ain
Figure2). Theseengrams areprimarily composed of prior olfac-
tory input patterns, accumulated through exposure to different
chemicalsandmixturesof chemicals. However, aswediscusslater
in this article, perceptual information fromother senses may also
beencoded in this store.
Assumption 4 (Pattern Matching)
Pattern matching in the olfactory processing module is proba-
bilistic, neither all-or-nonenor exclusive. A givenolfactory input
maymatchandhenceactivatemanyengramstoagreater or lesser
extent, andthispatternof activationsmayvarysomewhat between
repeat presentations of the same stimulus. In addition, there is
likely tobesomedegreeof mutual inhibitionbetweenengramsso
that if one particular engramis strongly activated, then this will
tendtoinhibit activationof other engramsthat wouldprovideonly
apartial match.
Assumption 5 (Encoding Purely Olfactory Engrams)
When an input pattern (Number 1 in Figure 2) fails to match
strongly with any stored engram, this provides theconditions for
encoding a new olfactory engram. The process of encoding in-
volves theoutput fromtheolfactory processor modulebeing fed
back to an automatic comparator and encoder (via Numbers 3
and 4 to Number 2b in Figure 2), where it is automatically
comparedwiththeolfactoryinput. Becausethetwowill notmatch,
thecontents of thecomparator areencodedas anewengramand
stored in theprocessing module.
Assumption 6 (Resistance to Interference)
When an input pattern closely matches an engramin the pro-
cessingmodule, encodingis prevented. This occurs inthefollow-
ing way: The processor output is again fed back (via the same
routeasinAssumption 5) totheautomaticcomparator andencoder
whereitiscomparedwiththeolfactoryinput. Becausethetwowill
broadly match, thecontents of thecomparator arenot encoded.
Assumption 7 (Encoding Composite Olfactory/Non-
Olfactory Engrams)
The store component of the olfactory processing module also
contains composite engrams composed of an olfactory and non-
olfactory component(s). Encoding composite engrams calls on a
further feature of the theory. When output from the olfactory
processor is fedback to theautomatic comparator andencoder, it
is fed back viatwo other modules: acontrolled associator that is
not relevant here(seeAssumption 11) andasensoryintegrator that
is relevant (Number 4 in Figure2). Thesensory integrator corre-
latesthearrival of olfactoryprocessor output withother perceptual
events. When two streams of perceptual information are tempo-
rally correlated they are fed back as a packet to the automatic
comparator andencoder (viathecontrolledassociator). Thepacket
is then compared with the olfactory input in the automatic com-
parator andencoder. Whentheolfactory component of thepacket
is familiar and hence similar to the olfactory input, encoding is
retarded. Whentheolfactorycomponentisunfamiliar, thecontents
of thecomparator areencodedintheprocessingmodule, resulting
in the formation of a composite engram of olfactory and non-
olfactory information.
Assumption 8 (Access Constraints on Engrams in the
Processing Module)
Bothpurely olfactory andcompositeengrams may beactivated
only whentheolfactory part of theengramisreexperiencedthat
is, content addressable memory. Hence recall of engrams in the
processing module can occur only via pattern matching from
olfactory input (Numbers 1 and 2ain Figure2).
Assumption 9 (Feelings of Familiarity)
Thefamiliarity of anodor is aproduct of thepattern-matching
process (Number 2a in Figure 2). Thus an input pattern that
matches fewengrams closely will bejudgedas less familiar than
an input pattern that has stronger matches.
Assumption 10 (Identification)
Thegreater theactivationof aparticular engramintheprocess-
ing module the greater the likelihood that it will excite an asso-
ciativelink or linkstosemanticor episodicknowledge(Number 5
in Figure 2). These associations can generate either partial (it
smells like some kind of herb) or complete (its oregano)
identification. This process is bothvariableandfallible. Anodor-
ant identifiedcorrectlyononeoccasionmayseemhighlyfamiliar,
but not identifiable, on thenext.
Assumption 11 (Acquiring Associations Between Semantic
and Episodic Knowledge and Olfactory Engrams)
Associations between an engram in the olfactory processing
module and episodic or semantic knowledge may occur when
output fromtheprocessor (Number 2 in Figure2) and theto-be-
associated information are both available to the controlled asso-
ciator (Number 3 in Figure 2). Such associations are effortful,
strengthened through repetition, and proneto interference.
Assumption 12 (Top-Down Influences)
Particular semantic or episodic knowledge may lower the
thresholdfor activationof individual or sets of relatedengrams in
theolfactory processing moduleviapreviously acquired associa-
tions (link betweenNumbers 5and2inFigure2). Thesemay act
tofacilitateidentificationof anodor. If it lookslikeanorange, and
feelsandtastesinthemouthlikeanorange, itsodor ismuchmore
likely to be identified as orange-smelling. Verbal information
alonemay play asimilar role: If toldbeforehandthiscouldsmell
347
A MNEMONIC THEORY OF ODOR PERCEPTION
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like an orange or a mushroom, a person will be more prone to
identify orangeodor asorangethanthey might if nosuchcuehad
been provided.
Assumption 13 (Imagery)
Thetheory suggests that experienceof odor quality is possible
onlywhenaninputpatternisavailabletothepatternmatcher inthe
processing module. Thus the only stimulus sufficient to activate
engramsintheolfactoryprocessingmoduleisaphysicallypresent
one, implying that odor imagery is unlikely (excepting perhaps
activationduringanepilepticauraor schizophrenichallucination).
Assumption 14 (Short-Term Storage and Recognition
Memory)
When an engramis activated, activation gradually decays but
lasts longer than both the offset of stimulation and the loss of
perception of the activating stimulus. Two consequences flow
fromthis. First, it allows for an apparent short-termstorage ca-
pacity, as a consequence of the activation of engrams in the
processing module. Thus facilitated identification of recently ex-
perienced odors is enabled in an analogous manner to that pro-
posedfor top-down priming, through loweringthethresholdnec-
essary to activate a particular engram (see Assumption 12).
Second, residual activation may ultimately last for a very long
time: days, weeks, or evenmonths. Thiswouldby necessity mean
relatively flat forgetting curves (from minutes to months) and
provide a mechanismfor olfactory recognition memory (see As-
sumption 12).
Commentary on theAssumptions
Commentary on Assumption 1 (Tabula Rasa)
Thetheory assumes that odors haveno inherent psychological
properties. This implies that neonates, infants, andchildren prob-
ably perceiveodor quality in adifferent manner fromadults and
that their hedonic responses differ as well. Although limited, the
available evidence supports this view. Starting with hedonic re-
sponses, Steiner (1979) suggested that neonates possess an auto-
maticresponsetocertainodors, typifiedbyafacial expressionakin
to that demonstrated when neonates samplethebitter tastant qui-
nine(seeSteiner, Glaser, Hawilo, & Berridge, 2001). Morecon-
sideredstudieshavefailedtoconfirmthisview. Althoughthereis
some limited evidence that infants a few hours old do show
dislikes for odors that adults also find unpleasant, thestrength of
this response is nowhere near as potent as that shown toward
quinine (Soussignan, Schaal, Marlier, & J iang, 1997). Because
olfactory exposure in utero is now known to alter preferences in
the neonate, it is difficult to eliminate the possibility that any
observed hedonic responsearises simply fromthis typeof expo-
sure(Schaal, Marlier, & Soussignan, 2000).
The hedonic responses of infants and older children to odors
present anequallymixedpicture. Althoughonestudyhasreported
evidenceof hedonic differencesinchildrenakintothoseinadults
(Schmidt & Beauchamp, 1988), doubts surroundits methodology
(Engen& Engen, 1997), andinaddition, other studieshaveshown
that such responses in this age group are highly sensitive to
experimental instructions (e.g., Strickland, J essee, & Filsinger,
1988). For the archetypal foul odor, feces, (Angyal, 1941), it is
difficult to reconcile Rozins observation (Rozin & Fallon,
1987)that young children will readily play with itwith the
notionof aninnatedislikefor its odor. This viewis supportedby
twofindings. First, Peto(1935) observedthat 89out of 92children
under 5yearsold, demonstratednosignof dislikeor disgust when
tested with putrefying and fecal odors. Second, Moncrieff (1966)
found that children werelargely indifferent to thefecal-likeodor
of skatole.
For odor quality the data are more limited. First, there are no
relevant studies conducted with children less than 5 years old.
Second, studiesof older childrenhaveexaminedonlytheabilityto
identify odors. Although identification calls on a variety of cog-
nitive processes, it is known to correlate substantially with dis-
criminative ability (De Wijk & Cain, 1994a, 1994b; Eskenazi,
Cain, Novelly, & Friend, 1983), and onewould thereforepredict
poorer odor identificationinchildren, ashasbeenobserved. Doty,
Shaman, Applebaum, et al. (1984) administeredtheUniversity of
PennsylvaniaSmell IdentificationTest (UPSIT; Doty, Shaman, &
Dann, 1984) to a large sample of participants (nearly 2,000) of
varying ages. The test involves smelling an odor and identifying
fromalist of namesthecorrect onefor that stimulus. Children59
yearsoldperformedsignificantly worseat recognitionthandidall
theolder samples up to theageof 70 years. Only adults aged 80
or more years performed worse. Similar findings have been re-
ported by Cain et al. (1995), De Wijk and Cain (1994a, 1994b),
andLehrner, Gluck, andLaska(1999). It is important tonotethat
Cainet al. (1995) didnot findanydifferencebetweenchildrenand
adultsinolfactory sensitivity, asmeasuredby astandardolfactory
threshold test. This suggests that differences in sensitivity are
unlikelytobethecauseof identificationdifferences. Finally, using
a different technique, Larjola and Von Wright (1976) found that
younger children(meanage5years) weresignificantlyworseat
recognizing odorants that they had just smelled than were older
children, both immediately and after a 1-month delay. Taken
together, thesestudiessuggestthatchildrenprobablyperceiveodor
quality in a different manner fromthat of adults and that such
differences are eliminated by progressive gains in olfactory
experience.
Commentary on Assumption 2 (Input Pattern)
The concept of a complex spatial and temporal pattern as the
neural representation of an odor is both widely accepted (e.g.,
Buck, 1996, 2000; Haberly, 1998; Laurent, 1999; Malnic et al.,
1999; Sullivan, Ressler, & Buck, 1995) andwell supportedexper-
imentally. According to this perspective, odors are encoded as a
complex patternof activationacrossthe1,0002,000glomeruli in
the olfactory bulb. The evidence for this assertion, which is dis-
cussedinmoredepthinthestudiescitedabove(andseetheearlier
section The Human Olfactory System), can be summarized as
follows: (a) Therearealargenumber of olfactoryreceptors(about
500750; Buck & Axel, 1991); (b) each receptor type is very
broadlytuned, respondingtoavarietyof differentchemical stimuli
(Malnic et al., 1999); and(c) informationfromeachreceptor type
is channeledonto specific glomeruli so that thepatternacross all
glomeruli is likely to differ between odors, even if thepattern of
activationfor aparticular receptor does not (Malnic et al., 1999).
348
STEVENSON AND BOAKES
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A further aspect of theinput patternconcerns howinformation
about odor intensity is recovered. We adopted Lansky and Ro-
sparss (1993) suggestion that intensity information is extracted
very early inolfactory processing. However, suchintensity infor-
mationmust requirefurther processingto account for effects like
sniff vigor constancy, whereby variations insniff depth, andthus
amountof odorantdeliveredtoreceptors, producelittlevariationin
odor intensity (Teghtsoonian, Teghtsoonian, Berglund, & Ber-
glund, 1978).
A further considerationiswhether intensityinformationfollows
thesameprocessing path as quality information. As noted in the
section on theeffects of brain injury that follows, it is very clear
that many suchconditionssparetheability toperceivedifferences
in odor intensity (particularly the case of H.M.; but see West &
Doty, 1995) whileeliminatingtheability to perceiveodor quality
(White, 1998). This suggests separate processing streams. How-
ever, onepuzzlingfindingis that factor analysis of different tests
of olfactory function do not typically separate out measures of
sensitivity fromthoseof quality perception, as might beexpected
(Doty, Smith, McKeown, & Raj, 1994). One possibility is that
adequate sensitivity is a necessary prerequisite for odor-quality
perception (thus variations in sensitivity will affect odor-quality
perception) but that the absence of odor-quality perception need
not affect sensitivity.
Finally, itiswell establishedthattheperceivedqualityof certain
odorants changes as their concentration is increased (Gross-
Isseroff & Doron, 1989; Moncrieff, 1951). Wenoteinpassingthat
such findings are easily accommodated within the theory on the
basis of changes in receptor binding, olfactory input, and thus
engrams activated.
Commentary on Assumption 3 (What Is the Pattern
Compared With?)
Thetheoryassumesthat thereisadedicatedolfactorystore(the
olfactory processingmodule) that receives input directly fromthe
olfactory bulb (i.e., glomeruli) and that stores previous input.
Evidencefor thisstructurecomesfromthreesources: (a) plausible
neuroanatomical correlatesof theolfactoryprocessingmodule(see
Neuroanatomical Basisof theTheory); (b) theneuropsychological
data, which suggest that memory and perception in olfaction are
indistinguishable(seeNeuropsychological Data); and(c) thepsy-
chological data, whichprovidesomeevidenceof aseparateolfac-
torystore. Thislatter assertion, whichisconsideredinthissection,
isbasedonfour typesof functional dissociation: (a) differencesin
resistancetointerference, (b) differences betweenolfactory mem-
ory and both implicit and explicit memory for other types of
stimuli, (c) theunusual difficulty that participants haveinnaming
odors, and (d) factor analytic studies of cognitive and olfactory
abilities.
Olfactory memory may be especially resistant to interference.
This has been suggested by two types of study: (a) thoseusing a
recognition-memory procedure, which show little forgetting of
olfactory stimuli over long delays (e.g., Engen & Ross, 1973;
Lawless, 1978; Lawless & Cain, 1975), and (b) processes pre-
sumedto reflect engramencoding, namely theresistanceto retro-
activeinterferenceof odortastelearning(Stevensonet al., 2000a,
2000b), and odorodor learning (Stevenson, Case, & Boakes, in
press). These conclusions need to be tempered, because interfer-
encemaytakeplaceunder certainconditions(seeCommentary on
Assumption 6), andalso other forms of stimuli, suchas free-form
shapesandfaces, mayshowsimilar effects(Lawless, 1978). None-
theless, as a general feature of a sensory system, such findings
appear to set olfaction apart.
A second unusual property stems fromtheapparent similarity,
but singular difference, between olfactory memory (i.e., the en-
gramstorein Figure2) and implicit memory. Implicit memory is
a blanket term describing situations in which prior experience
affects performance without requiring intentional recollection
(Schacter, 1987). Several parallels betweenimplicit andolfactory
memoryexist, includingeffortlessandrapidacquisition(DeSchep-
per & Treisman, 1996), resistance to interference (e.g., Graf &
Schacter, 1987), andtheintegral natureof perceptionandimplicit
memory (e.g., J acoby, Allan, Collins, & Larwill, 1988). Implicit
memory for stimuli inother modalities is generally unaffectedby
aging, by Alzheimers disease (e.g., Winograd, Goldstein, Mon-
arch, Peluso, & Goldman, 1999), by Korsakoffs syndrome(e.g.,
Benzing& Squire, 1989; Nissen, Willingham, & Hartman, 1989),
or by temporal lobectomy (Gabrieli, Milberg, Keane, & Corkin,
1990). Incontrast, olfactory memory isprofoundly affectedby all
the above conditions, as is explicit memory for stimuli in other
modalities, as discussed below. Theimplication fromthis is that,
althougholfactory memory shares morefeatures incommonwith
implicit thanexplicit memory, it differsintheneuropsychological
conditionsthat affect it, settingit apart fromitsclosest theoretical
classification.
A thirddifferenceconcerns thedifficulty that adult participants
havein naming even common odors, when other cues areabsent
(e.g., Cain, 1979; Desor & Beauchamp, 1974; Larsson, 1997;
Lawless & Engen, 1977). This suggests that odor memory is in
somewaydifferent fromstoresof visual information, for example,
wheresuchdifficulties arerare(e.g., Cainet al., 1995). Finally, a
recent factor analytic study of cognitive (e.g., verbal, tonal and
symbol memory, IQ, executive function) and olfactory abilities
(e.g., odor memoryandidentification; Danthiir, Roberts, Pallier, &
Stankov, 2001), revealed that odor memory was a structurally
independent factor. Takentogether, thesefour setsof observations
support thenotionof apsychologically discreteolfactory memory
system, which here forms the engramstore of the olfactory pro-
cessing module.
Commentary on Assumption 4 (Pattern Matching)
A key information-processing step in the theory is pattern
matching between theolfactory input fromtheglomeruli and the
engramstore. Support for this notioncomes frombothneuroana-
tomical data (see Neuroanatomical Basis of the Theory) and ex-
perimental psychology.
Although amatching-typeprocess has been alluded to by sev-
eral authors (see Dodd, 1988; Ohloff et al., 1991; Polak, 1973;
Schild, 1988), its ability to account for the learning data (e.g.,
Stevenson, 2001a, 2001b, 2001c; Stevenson et al., 1998) is what
initiallyledustosuggest it. Inparticular, matchingatarget odors
input withpreviously encodedengrams typically leads tothetype
of findingobtainedinour learningstudies. For example, smelling
lychee after lycheesucrose pairings leads to the recovery of a
lycheesucroseengramby virtueof theengrams similarity to its
input.
349
A MNEMONIC THEORY OF ODOR PERCEPTION
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Thematchingprocessisalsosupportedby itsability toaccount
for anumber of other findings. Thefirst istheabsenceof primary
odor qualitiesdescribedearlier. Settingasidethefact that multiple
nonspecific receptors have been unambiguously identified (e.g.,
Buck, 2000), themnemonictheoryplacesnoboundsonthetypeor
number of qualitiesthat maybeexperiencedother thannotingthat
richness of olfactory experience should increase as a function of
exposureto newodors.
A second finding is the role that similarity appears to play in
judgments of odor quality (Lawless, 1999). Exactly such a rela-
tionship would beexpected by our theory, in that when apartic-
ipant isaskedtocompareanodor toaseriesof qualitydescriptors
thisprocessisanalogoustothat of odor perception, exceptingthat
theformer occursinserial, whereasthelatter occursinparallel. It
is this important difference that we believe separates the experi-
enceof anodor indaily lifefromthat reportedby ratingqualities
in thelaboratory.
A thirdfindingistheconsistentlyimperfect correlationbetween
quality andchemical structure(e.g., Boelens, 1974; Polak, 1973),
regardless of the type of structural feature chosen for analysis.
Althoughsuchfindingsareaproblemfor any particular structure-
quality model, they do not pose a problemfor matching-based
theoriessuchastheoneproposedhere. Thisisbecauseamatching-
based theory can comfortably accommodate any type of feature-
based model (i.e., it is complementary). This follows from the
principle that similarity of glomerular layer input to the theory
(i.e., resulting fromsimilar binding patterns of odorant to recep-
tors) will produce similar patterns of activation in the olfactory
processing moduleand thus asimilar odor-quality percept.
Fourth, theprocess of patternmatchingembraces thenotionof
redintegration (Horowitz & Prytulak, 1969), in which apart of a
complex whole can recover its totality. Such effects have been
observed in both rat and human participants. In rats, extensive
lesions of theglomerular layer, includingthoseparts knowntobe
most active for a target odorant, do not prevent appropriate re-
spondingtoodor-stimulusrelationshipslearnt earlier intheexper-
iment (Lu & Slotnick, 1994; Slotnick, Bell, Panhuber, & Laing,
1997). This suggests that even afragmentary input may besuffi-
cient to recover thewhole. In humans, redintegration can best be
demonstrated with odortastelearning, in that asniffed odor can
recover an engramthat includes theexperienceof that odor with
sucrose(e.g., Stevenson et al., 1995).
Finally, the very process of pattern matching should make it
difficult to dissect complex odor mixtures into their individual
components(Haberly & Bower, 1989). That is, eachinput pattern
will largely be treated as a unique stimulus, even when it is a
mixture of several chemicals, as most odors are. In humans,
exactlythisphenomenonhasbeenobserved. Inanextensiveseries
of investigations, Laing and colleagues (e.g., Laing & Francis,
1989; Livermore & Laing, 1998a, 1998b) have established that
ordinary participants, and even experts such as perfumers and
flavorists, are unable to identify more than two or three compo-
nents in an odor mixture.
Commentary on Assumption 5 (Encoding Purely Olfactory
Engrams)
Two types of evidencesuggest that anovel odor is encodedin
aspecial storeandthat thisencodingmodifiessubsequent percep-
tionof theodor. Thefirsttypecomesfromtheexperimentsonodor
learning that we reviewed earlier. The second type of evidence
comes fromstudies showingthat themereact of smellinganovel
odor is sufficient to improveits discriminability fromother novel
odors, an observation that until now has had no theoretical basis
(J ehl et al., 1995; Rabin, 1988; Rabin & Cain, 1984). This effect
has been most clearly demonstrated by Rabin (1988), who found
that preexposing participants to a set of odors enabled themto
discriminatebetweenmembersof that set significantly better than
non-preexposed controls. Such an outcome can be directly ac-
countedfor by thetheory. Oneshouldrecall that whenanodor is
first smelled, particularly if it is not that familiar (as in Rabin,
1988), theodor will matchfewengramsintheolfactoryprocessor,
thus producing far less activation of any individual engramthan
will a familiar odor. Three consequences should flow fromthis.
First, anovel odor will smell of multiplequalitiesrather thanbeing
primarilycharacterizedbyonequalitytheconsequenceof lotsof
partial activation of slightly to moderately similar engrams. This
suppositionwassupportedinarecent study by Stevenson, Demp-
sey, andButton(2003), whofoundthatnovel odorsweredescribed
as having more qualities, of lesser similarity to the target, than
familiar odors. Second, odorsthat areunfamiliar will alsobemore
confusable(e.g., Rabin, 1988), asadirect consequenceof thefirst
point. Third, anovel odor, initially producingpartial activationof
many engrams, should with further exposure be encoded in the
engramstore. Thus, onsubsequent encounters, thetarget odor will
come to activate its own previous encoding, hence limiting its
pattern of reported qualities and enhancing its distinctiveness.
Commentary on Assumption 6 (Resistance to Interference)
Thetheory proposes that when afamiliar odor is encountered,
no further encoding of that odor will take place in the olfactory
processingmodule. (Oneshouldnotethat thisdoesnot excludethe
formation of explicit associations between engrams and semantic
or episodic knowledgemediatedby thecontrolledassociator). As
we discussed earlier (see Assumption 4), experimental data are
largely in accord with this view. First, odortasteand odorodor
learning are resistant to interference (Stevenson et al., 2000a,
2000b; Stevensonet al., inpress). Second, odor-recognitionmem-
oryhasbeendemonstratedinseveral studiestobeparticularlylong
livedand thus presumably resistant to interference(e.g., Engen
& Ross, 1973; Lawless & Cain, 1975; Lawless & Engen, 1977;
Rabin & Cain, 1984).
The theory, however, does allow some interference to occur
under twoconditions. First, whenanodor ismoderately similar to
an existing engram, some encoding of the target will eventuate.
This may explain why odorodor learning effects are typically
small, onthebasis that onemember of thepair is oftenafamiliar
odor (e.g., cherry), whereastheother isnot (e.g., p-anisaldehyde).
Thecombination(p-anisaldehydecherry) maythereforeresemble
theengramof thepreviously encountered odor (e.g., cherry) and
thusretardbut not preventacquisitionof thecombination(see
Stevenson, 2001c). Thesecondtypeof interference, alsoafunction
of similarity, canoccur duringrecognition-memory tasks, andthis
is discussed separately in Commentary on Assumption 14.
350
STEVENSON AND BOAKES
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Commentary on Assumption 7 (Encoding Composite
Olfactory/Non-Olfactory Engrams)
Thetheory uses two different forms of learning. Thefirst type
of learning is theencoding of information in theautomatic com-
parator andencoder intotheengramstore, whichmayincludeboth
olfactory (see Assumption 5) and composite olfactory/non-
olfactory information. This type of learning, which we have re-
ferredtopreviouslyasconfigural (Stevensonet al., 1995, 1998), is
envisaged to be relatively fast, effortless, long-lasting, and resis-
tant to interference. The second form of learning involves the
formation of associations between the contents of the controlled
associator. Thismight involvelearningthat anodor comesfroma
particular source, learninginformationabout theodor, or learning
the odors name (e.g., Davis, 1977; Rabin, 1988). In this case
learning is relatively slow, effortful, and proneto interference.
Because parsimony would demand one learning system, it is
necessary to justify the need for two. The best justification is to
contrast two forms of learning that are known to involve odors:
odortastelearningandodorshocklearning. Inodorshocklearn-
ing olfactory cues areused to predict theonset of electric shock.
Learning in this paradigm resembles that found in many other
studies of human associativelearning, with acquisition occurring
only with conscious awareness of the contingencies and rapid
extinctionoccurringwhenparticipantsrealizethat theodor cueno
longer predicts shock (Marinkovic, Schell, & Dawson, 1989; and
seeVan den Burgh et al., 1999, for similar findings and Dawson
&Schell, 1987, for general discussionof thepropertiesof thistype
of learning).
Odortaste learning, as described earlier, appears to possess
very different properties. It involves fast acquisition (Prescott,
1999) withapparently nonecessity for participants tobeawareof
the experimental contingencies (Stevenson et al., 1998) and in-
volves so vivid a recollection of the taste component that the
experienceprobablycountsassynesthetic(Stevensonet al., 1998).
Inaddition, suchlearningdemonstratesbothlatentinhibitionunder
no-maskingconditions (Stevenson & Boakes, in press) andresis-
tanceto retroactiveinterference(Stevensonet al., 2000a, 2000b).
Thetwoseparatelearningsystemsusedinthetheoryallowthese
differences to be explained. A controlled associator is necessary
for odor shock or relatedforms of learning, inwhichcontingency
awarenessmust beachievedprior toany changeinbehavior (e.g.,
Shanks & St. J ohn, 1994). However, if no association is formed
and information is treated as a configuration (one entity), then
thereis no necessity for acontrolled associator. It is under these
conditions that the second learning process operates, with infor-
mation being encoded as an engramin the store. The properties
that this process of learning has are unusual because it does not
rely on the formation of associations. Consequently, learning is
relatively fast and effortless, and theresulting engrams areresis-
tant to interference because of the access restrictions that we
described earlier (i.e., content addressableonly).
The automatic comparator and encoder can also process
olfactory/non-olfactoryengrams, suchasthat betweenanodor and
ataste. Thereis, however, no reason why other forms of sensory
informationcouldnot beco-storedinthesameway, andpresum-
ably such composite engrams would possess similar properties
(seeHaberly, 2001, for asimilar suggestion). Thesewouldinclude
thefollowing: (a) resistancetointerferenceandthuslongevity, and
henceretrieval onlyviatheodorouscomponent of theengram; (b)
vividness, as with the taste component of odors; and (c) third,
emotiveness, aswithall odor stimuli. Preciselysuchqualitieshave
been identified in a series of studies on odor-induced memories
(Chu & Downes, 2000a, 2000b), which have demonstrated their
vividness, longevity (often fromchildhood), and emotiveproper-
ties. It is suggested here that these so-called Proustian memories
emergeasaconsequenceof their storageascompositeengramsin
theolfactory processing module.
Finally, odorsareknowntobeinvolvedinonetypeof memory
phenomenon that may be harder to reconcile with the format
adopted here. This concerns using odors as a contextual cue.
Several demonstrations have been made of this effect, whereby
recall is facilitated when the olfactory context present during
learning is reinstated at test (e.g., Cann & Ross, 1989; Pointer &
Bond, 1998). As we have argued, associations between an odor
and alabel requiresomeeffort to form, yet in thesestudies odor
waspresent asanincidental cuehardlyanideal situationtoform
associative links between the odor and the to-be-remembered
information(e.g., wordsor faces). Oneexplanationof sucheffects
is given by the encoding-specificity account (Tulving, 1983), in
whichall availablecuespresent duringlearningbecomepart of the
trace, thus the presence of such cues during recall will assist
retrieval. Thisaccountpresentsaproblemfor thepresenttheory, in
that it assumes storagein acommon memory systemunder con-
ditions inwhichonewouldnot expect this to occur. Onepossible
resolutionof thisproblem(seeCann& Ross, 1989; Epple& Herz,
1999; Herz & Engen, 1996) is to assume that this effect is not
mediatedthroughtheodor per sebut throughthemoodor arousal
state that an odor may invoke during testing. Thus the odor acts
only indirectly as aretrieval cueby reinstating themoodarousal
level present during learning. However, one should note that the
claimthat moodcanact asacontextual cueisitself controversial.
Commentary on Assumption 8 (Access Constraints on
Engrams in the Processing Module)
As we noted earlier, the contents of the engramstore can be
accessed only by the physical presence of an odorant (content
addressable memory). Apart from the implications for limiting
interference (see Commentary on Assumption 6), it also has im-
portant ramifications for odor imagery, whicharediscussedlater.
Commentary on Assumption 9 (Feelings of Familiarity)
The degree to which an odor feels familiar or novel appears,
alongwithits intensive, qualitative, andemotional dimensions, to
beanintrinsic part of odor perception. For example, Lawless and
Engen (1977) found that response latencies were shortest when
participants were asked to judge the familiarity of an odor. Ac-
cordingto thetheory, familiarity is consideredto beafunctionof
thedegreeof engramactivation in theolfactory processing mod-
ule. Fromthisperspective, anodorsfamiliarity, aswithitsquality,
will not beaffected by whereit is smelled or by thefact that the
participant may not be able to identify either the name or place
where the odor was last encountered. Familiarity is therefore an
emergent property of theolfactory processing module.
351
A MNEMONIC THEORY OF ODOR PERCEPTION
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Commentary on Assumption 10 (Identification)
As wenotedearlier, odors, evenfamiliar ones, canbedifficult
to name (e.g., Cain, 1979; Desor & Beauchamp, 1974; Larsson,
1997; Lawless & Engen, 1977). The theory accounts for poor
naminginthreeways. First, odornameassociations may initially
be hard to formcompared with other senses (e.g., Davis, 1977).
This is because olfactory memory (the processing module) is a
discrete entity with a paleocortical location (Haberly, 1998; see
Neuroanatomical Basis of the Theory for further discussion) and
thusphysically distant fromthelikely (neocortical) siteof seman-
tic and episodic memory (see also Herz & Engen, 1996, for a
discussion of other potential ramifications of olfactions unique
anatomy). Second, thematchingprocessbetweentheinput andthe
storedengrams is assumedtobeprobabilistic (seeAssumption 4);
consequently, evenfamiliar odors may occasionally bemisidenti-
fied(i.e., thewrongengramor engrams activated), leadingto the
productionof anincorrect name(e.g., Cain& Potts, 1996). Third,
theactivationof associationstosemanticmemoryisalsopredicted
to be probabilistic; thus, increasing the number of engrams acti-
vated should make category-level identification relatively easy
(e.g., itsafruit). However, familiar odors, withfewer but more
strongly activatedengrams, may bevulnerableto anomiabecause
of thegreater impact of theprobabilisticnatureof activationonthe
limited number of name-specific associations.
Commentary on Assumption 11 (Acquiring Associations
Between Semantic and Episodic Knowledge and Olfactory
Engrams)
Commentary on the formation of associations between odors
and semantic or episodic knowledge is discussed under
Assumption 7.
Commentary on Assumption 12 (Top-Down Influences)
Thetheory suggests that semantic or episodic knowledgemay
facilitateodor identificationby loweringtheactivationthresholds
of engrams in the olfactory processing module (i.e., olfactory
priming). The only direct evidence for this notion comes froma
studybySchabandCrowder (1991), whoobtainedpriminginonly
oneof four reportedexperiments. Usingfamiliar odors, Schaband
Crowder found that preexposure to an odors name alone facili-
tatedcorrect identificationwhenthat odor waspresentedinalater
identification task, in comparison with a no-preexposure control.
Althoughit is difficult todrawstrongconclusions fromthis study
becauseof Schab and Crowders failureto replicatetheir results,
thestudy suggests that havingbeenpreviously exposedtoaname
canlater benefit aparticipants ability to identify anodor bearing
that same name. Other evidence on top-down influences comes
fromresearch on wine tasting. A white wine that is artificially
colored red is misperceived as having features that are more
appropriateto red wine(Morrot, Brochet, & Dubourdieu, 2001).
Commentary on Assumption 13 (Imagery)
Thetheory suggests that odor imagery is unlikely becauseonly
physically present stimuli caninitiateaccess totheolfactory store
and hence activate engrams. Theory aside, empirical support for
odor imagery is weak. There are four types of study. The first
simply asks participants howclear and vivid their mental images
arefor eachof thedifferent senses. Betts(1909), Sheehan(1967),
andLawless (1997), amongothers, all report that thevividness of
olfactory images is considerably less than images from other
sensorymodalities, includingtaste. A secondapproachhasbeento
ask participants to judge similarities between pairs of odorants,
somein areal and others in an imagined condition, and then use
multidimensional scaling to examine the odor space created for
each dataset (Carrasco & Ridout, 1993). Although Carrasco and
Ridout (1993) concluded that imagery was present for olfaction,
theycouldnotruleoutverbal mediationintheimagerygroupasan
explanation (i.e., responses based on what the participant knows
about odors). More troubling still, in their multidimensional-
scaling solution the pleasantnessunpleasantness dimension that
usually emerges as theprincipal dimensionfor odors (Schiffman,
Robinson, & Erickson, 1977) was observed in the perceptual
conditionbut not intheimagery condition. Thisisvery surprising
given that the affective quality of odors is one of their defining
characteristics (Richardson & Zucco, 1989).
A third approach is to ask participants to imagine combining
chemosensory stimuli and then report on therelativeintensity of
the components (e.g., Algom & Cain, 1991). Algom and Cain
(1991) reported that following such a request, participants per-
formedinthesamewayaswhenpresentedwithreal mixtures. This
typeof claimhasbeenchallengedbybothSchifferstein(1999) and
by Stevenson and Prescott (1997) on two grounds. First, partici-
pants do haveconsiderableexplicit knowledgeabout howcertain
mixtureswill behaveandthisknowledgeappearstobeusedinthe
imagery condition. A second criticism is that a more refined
analysis shows that thepattern of results obtained under imagery
conditions fails to match thosefromdirect perception.
A fourthtypeof study wasperformedby LymanandMcDaniel
(1990), whofoundthat aconditioninwhichparticipantsimagined
smelling items froma word list produced better subsequent rec-
ognition of those actual odors than did a condition in which
participantswereaskedtovisualizethelist items. Althoughthisis
themostconvincingdemonstrationof olfactoryimagery, ithastwo
problems that cloud its interpretation. First, it is plausible that
verbal rehearsal underlay enhancedrecognitionintheodor imag-
ery group(i.e., repeatedly sayingtooneself Imaginethesmell of
banana,etc.). LymanandMcDanielsexperimentcouldnotdetect
this sort of non-olfactory facilitatory effect, because no verbal-
rehearsal (i.e., auditory imagery) control groupwas run(Schab&
Crowders, 1991, primingexperiment suggeststhat thisisnot idle
carping). Second, participants in the odor and visual-imagery
groupssurprisinglyreportedequal successincreatingtheir respec-
tive type of image. This stands in marked contrast to other phe-
nomenological reports (see above). In conclusion, taking all the
odor-imagery studies together and contrasting them with other
sensory systems (see Richardson, 1999), at best it may be con-
cluded that theevidencefor olfactory imagery is weak.
Commentary on Assumption 14 (Short-Term Storage and
Recognition Memory)
The theory suggests that activation of an engram may last
beyonditsconsciousperception. Thishastwoconsequences. First,
it allows for a form of olfactory short-term storage, which is
neither functionally nor structurally separate fromthe long-term
352
STEVENSON AND BOAKES
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engramstorebut rather a consequenceof its activation (e.g., see
Cowan, 1988, for discussion of similar models of memory). Sec-
ond, this residual activation may be very long lived, providing a
mechanismfor odor-recognition memory.
There is currently no consensus on whether there is a discrete
olfactory short-termstore(of any type). Traditionally, four types
of evidencehavebeenpresentedtoestablishadistinctionbetween
along- andashort-termstore: capacity differences, codingdiffer-
ences, neuropsychological differences, and serial position effects
(White, 1998). Given thetypeof short-termstoreproposed here,
thereshould beno capacity difference, no coding difference, and
no evidence of any neuropsychological dissociation. Serial posi-
tion effects areamorecomplex issue, becausethereis consider-
able uncertainty about their implications for dissociable memory
systems (e.g., Baddeley & Hitch, 1993).
Inapparentcontradictiontoour predictions, theredoesappear to
besomeevidencefor capacity differencesinolfaction. Short-term
recognition performance decreases as the number of odors to be
remembered on a given trial is increased (Engen, Kuisma, &
Eimas, 1973; F. N. J ones, Roberts, &Holman, 1978). Thecapacity
of long-termmemory for odors is certainly large. Participants are
able to recognize, even after a 1-month delay, about 70% of a
48-odor set (Engen & Ross, 1973), and this level of recognition
appears to be independent of set size. This is, however, not the
wholestory. Althoughincreasingthenumber of stimuli increases
thenumber of itemsthat must beretained(i.e., testingcapacity), it
also increases thelikelihood of odors sharing similar characteris-
tics (e.g., being fruit-like). According to the theory, this should
disrupt recognition performance, becausewhen similar odors are
used they tend to activate overlapping engrams, making identifi-
cation more difficult (i.e., interference based on similarity). Be-
cause the detrimental effects of similarity have been observed
followingbothshort andlongdelays(Engen& Ross, 1973; J ehl et
al., 1994), capacity-differenceclaimsneedtobetreatedwithsome
caution.
Differencesincodingbetweenshort- andlong-termstoreshave
not beenadequatelydemonstratedinolfaction. Althoughevidence
for both perceptual and semantic coding has been obtained in a
number of experiments (e.g., Cain, De Wijk, Lulejian, Schiet, &
See, 1998; Cain& Potts, 1996; J ehl, Royet, & Holley, 1997), there
is no link between any particular typeof memorylong termor
short termandthecodingused. As for neuropsychological data,
these provide no definitive evidence for a distinction between a
short- and a long-termstore (see Mair, Harrison, & Flint, 1995;
White, 1998). Finally, recency and primacy effects have been
obtainedusingarecognitionprocedure(Reed, 2000). However, as
we noted above, it is difficult to assess the implications of such
findings. Taken together, these results provide little support for
any form of discrete short-term store. Rather, they suggest a
capacity to hold olfactory information, for either short or longer
periods, by virtue of residual activation. This process appears
sensitivetointerference, onthebasisof thesimilarity of theitems
in thetest set.
General Comments on the Assumptions
These have been developed in an attempt to accommodate
withinasingletheoretical frameworkarangeof findingsthat were
previously seen as unconnected. Thesefindings includepoor dis-
criminability of novel odorants, lack of primary qualities, imper-
fect correlations between structure and quality, effects of past
experience on odor perception, and current understanding of the
olfactory transduction process. As should beclear fromthecom-
mentsonspecificassumptions, for sometheempirical basisiswell
established but for others it is still quite fragile. Two further
sources of data that have an important bearing on the theory are
considered next: (a) whether the proposed systemis compatible
withcurrent neurophysiological findings andcanbemappedonto
different parts of thebrain, and(b) theextent to whichthetheory
provides a better understanding of abnormalities of odor percep-
tion following brain damage.
Neuroanatomical Basis of theTheory
Inthis sectionour aimis twofold: first, to demonstratethat our
model is broadly compatiblewithcurrent knowledgeinthis area,
andsecond, todrawexplicit parallelsbetweentheprocessingunits
outlinedinthetheory andparticular brainstructures. Twocaveats
are necessary. First, we make no attempt to provide a detailed
overview of olfactory neuroanatomy but instead concentrate on
consensus findings (see Savic, 2001, for review). Second, we
assume at this point some broad parallels between rat, monkey,
andhumanbrainsinolfactory neurophysiology andanatomy. The
validity of this assumption will beexamined in thenext section.
Thegrossneuroanatomyof theolfactorysystemisillustratedin
Figure3. Wedescribedearlier theprocessof transductionandthe
organization of primary information processing in theglomerular
layer of theolfactory bulb. This informationpasses fromthebulb
into theolfactory tract, which then splits into threebranches: the
lateral, medial, andintermediate(Heimer, VanHoesen, & Rosene,
1977). Thelateral branchisthemost important andprojectstothe
entorhinal andpiriformcortex andtheamygdaloidcomplex, all of
whichareprimarilylocatedinthetemporal lobe(J ones-Gotman&
Zatorre, 1993). Inaddition, thepiriformcortex alsoextendstothe
posterior orbitofrontal surface of the frontal lobe (Eslinger,
Damasio, & Van Hoesen, 1982). Three important sets of projec-
tions stemfromthese olfactory paleocortical areas: to the hypo-
thalamus, to the mediodorsal nucleus of the thalamus, and to
prefrontal cortex (Haberly, 1998). Theselatter two structures also
project to each other, and the prefrontal cortex has reciprocal
projections back to the piriformcortex. Four of these structures
appear toplayanespeciallyimportant roleinolfactoryperception,
learning, and memory. Thesearetheolfactory bulb, thepiriform
cortex, prefrontal cortex, and the mediodorsal nucleus of the
thalamus. Theroleof eachstructureanditspossiblemappingonto
our theory forms theremainder of this section.
The key element of our theory is the olfactory processing
module. Its neuroanatomical correlatewould beabrain structure
(or structures) that (a) receives information directly from the
glomeruli or related bulbar structures, (b) has appropriate neural
architectureto makemultiplecomparisons of this incominginput
with that stored from previous smelling episodes, and (c) has
appropriateconnections to other olfactory-relatedbrainstructures
for both the onward flow of information and reciprocal connec-
tions back for learning. Threestructures, either individually or in
combination, might fill thisrole: piriformcortex, prefrontal cortex,
and theolfactory bulb. Each is considered in turn.
353
A MNEMONIC THEORY OF ODOR PERCEPTION
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The piriformcortex has a number of features that make it a
plausible(if not themost promising) neural correlateof theolfac-
toryprocessingmodule. Thesefeatures, whichareoutlinedbelow,
haveledseveral researchers to suggest that thepiriformcortex is
aparadigmatic exampleof content-addressablememory, that is, a
systemfunctionally analogous to theolfactory processingmodule
proposed in our theory (see Barkai, Bergman, Horwitz, & Has-
selmo, 1994; Haberly, 2001; Haberly & Bower, 1989; Hasselmo,
Anderson, & Bower, 1992). The features that suggest it as a
putativeolfactory processing moduleareas follows:
1. Lesions of the piriform cortex can retard odor-
discrimination learning in rats (Slotnick & Schoonover,
1992).
2. Small areas of thepiriformcortex receiveinput fromall
areas of the olfactory bulb (Haberly, 1985), although a
recent tracingstudy inmicesuggests someorganization,
albeit withconsiderableconvergenceof multipleglomer-
uli output to multiplepoints inthepiriformcortex (Zou,
Horowitz, Montmayeur, Snapper, & Buck, 2001).
3. Many cells within the piriformcortex respond to olfac-
tory stimulation during single-unit recording (Haberly,
1969), and the structure is metabolically active during
olfaction (Sharp, Kauer, & Shepherd, 1977).
4. Thepiriformcortexreceivesinputfromprefrontal cortex,
allowing for the co-storage and association of informa-
tion fromother sensory systems (Haberly, 1985).
5. Major projections from the piriform cortex go to the
prefrontal cortex andthalamic structures, whicharealso
involved in olfactory discrimination and learning (see
below for a more detailed discussion; see also Schoen-
baum& Eichenbaum, 1995).
6. Inhumans, several neuroimagingstudies havefoundthe
piriformcortex active during smelling (for review, see
Doty, 2001).
7. Olfactory identification ability, as measured by the
UPSIT, is correlated with activity in thepiriformcortex
(Kareken et al., 2001).
The neural architecture of the piriform cortex also lends
itself to the type of pattern matching and storage systemthat
would be required by the olfactory processing module. Input
fromthe olfactory bulb via the lateral olfactory tract (see the
discussion above) synapses onto the top of a series of vertical
pyramidal cells. Thesecells areorganizedinlayers, withlower
levels containing separatelocal inhibitory and excitatory inter-
connections. In this model of piriform cortical function, the
pyramidal cell layers formthe neural basis of the odor store,
with engrams stored in adistributed fashion across thesecells.
It is important tonotethat thesecells demonstratetheplasticity
necessary for this role, inthat they showbothlong-termpoten-
tiation (Kanter & Haberly, 1993) and increased spine density
following olfactory learning (Knafo, Grossman, Barkai, &
Benshalom, 2001).
Figure 3. Schematicrepresentationof olfactorypathwaysinhumans. Olfactorycentersrepresentedincludethe
following: olfactory bulb(OB), lateral olfactory tract (LOT), olfactory tubercle(OT), anterior olfactory nucleus
(AON), piriformcortex(PC), entorhinal cortex(EC), amygdaloidcomplex(AC), hypothalamus(Hy), hippocam-
pal system (Hi), mediodorsal nucleus of the thalamus (MD), and orbitofrontal cortex (OFC). From The
Neuropsychology of Odor Memory, by R. Mair, L. M. Harrison, andD. L. Flint, inMemory for Odors (p. 47),
1995, Hillsdale, NJ : Erlbaum. Copyright 1995 by Erlbaum. Reprinted with permission.
354
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The evidence presented above is broadly supportive of the
piriformcortex as a neural correlate of the olfactory processing
module. However, some recent human functional magnetic reso-
nance imaging (fMRI) and rat neurophysiological data raise im-
portant issues that warrant comment. In particular, one human
fMRI study has found that the piriform cortex is activated by
sniffingodorless air andthat this activationis correlatedwiththe
degreeof sniff vigor (Sobel et al., 1998). Inaddition, bothhuman
fMRI (Sobel et al., 2000) and single-cell recordings from the
piriform cortex in rats (Wilson, 1998, 2000), suggest that the
piriformcortex adapts fairly rapidly to repeated presentations of
the same odor. It is important to note that Sobel et al. (2000)
showed that detection of the presence of an odor on a particular
trial could occur without significant activation in the piriform
cortex. Moreover, several humanfMRI studies havefailedtofind
activation here (see Zald & Pardo, 2000), a result Sobel et al.
(1998) attributed to rapid habituation and variations in control
procedures that may or may not include odorless sniffing. Al-
thoughall of thesefindingscanbereadilyaccountedfor (e.g., that
activationdoesnot alwaysequatewithprocessingandthat sniffing
acts as theattentional spotlight of olfaction), they do suggest the
need for caution before one may firmly conclude that primary
olfactory processing occurs here.
The prefrontal cortex has also been identified as an important
olfactory processing center. Prefrontal cortex (especially Brod-
manns Area 11) receives input directly from the bulb, from
several areasof olfactorycortex, andfromthemediodorsal nucleus
of thethalamus (Haberly, 1998). Lesions of theseprefrontal areas
in rats produce deficits in olfactory discrimination learning
(Eichenbaum, Shedlack, &Eckmann, 1980), withlesionedanimals
takingbetween3and4timesasmanytrialstoreachcriterioninan
olfactory go/no-go discrimination task. Single-cell recordings in
monkeyprefrontal regionshavealsoidentifiedprefrontal cortexas
a convergence site for information from olfactory and non-
olfactory sources (Rolls & Baylis, 1994), with single-cell record-
ingsindicatingolfactoryandvisual andolfactoryandtaste-specific
cells. Finally, human neuroimaging studies find prefrontal cortex
activatedinmany different odor-processingtasks (Cabeza& Ny-
berg, 2000).
In terms of neural correlates of the theory, we suggest that
prefrontal cortical regions may have more features akin to the
controlledassociator thantotheolfactoryprocessingmodule. This
suggestionismadefor several reasons. First, single-cell activityin
rat prefrontal regionsduringanolfactory discriminationparadigm
isvirtually identical tothat of thepiriformcortex (Schoenbaum&
Eichenbaum, 1995). The theory would predict such parallelism,
becausetheolfactory processingmoduleshouldproject thisinfor-
mation to the controlled associator (see Figure 2). Second, pre-
frontal areas are believed to be involved in the association of
on-going sensory input (Fuster, 2000; Schoenbaum & Eichen-
baum, 1995). Thisisessentiallytherolethat wehaveidentifiedfor
thecontrolledassociator, andit is well demonstratedinRolls and
Bayliss (1994) findings described above. Third, damage to pre-
frontal regions produces deficits in human participants ability to
extinguish acquired responses (e.g., Rolls, Hornak, Wade, &
McGrath, 1994). Becauseassociations producedby thecontrolled
associator are, according to the theory, sensitive to interference,
this would also suggest a further functional correspondence.
Fourth, prefrontal cortex (Brodmanns Area 11) is known to be
involvedintheformationof associationsbetweennamesandfaces
(Herholz et al., 2001), aprocessthat mayparallel theonebetween
names and odorsanother function attributed to the controlled
associator.
A further candidatestructurefor theolfactory processingmod-
uleistheolfactorybulb. Althoughthebulbhas(a) theinformation
necessary for such processing, (b) the capacity to demonstrate
learning (Shepherd & Greer, 1998), and (c) direct connections to
prefrontal cortexandolfactorycortex(Shepherd& Greer, 1998), it
is questionablewhether it has thenecessary neuronal architecture
to store olfactory (and presumably non-olfactory) information.
However, thepossibilitythat thebulbmayplaythisrolecannot be
excluded, and its role in olfactory learning and memory requires
further elaboration.
A final structurethat has demonstratedimportanceinolfactory
learningandmemory is themediodorsal nucleus of thethalamus.
Mediothalamic structures are known to be involved in (a) the
correlation of sensory information fromdifferent perceptual sys-
tems, (b) learning, and(c) memoryretrieval (Lezak, 1995). Inrats,
lesions to the mediodorsal thalamus lead to impaired olfactory
learning, although not as severe as those following prefrontal
lesions(Eichenbaumet al., 1980). Inaddition, suchlesionstendto
manifest behaviorally during more complex learning tasks only.
Montaldi andParkin(1989) suggestedthat mediothalamic deficits
result fromthebreakdownof theuseof contextual cuesinlearning
and retrieval. Precisely this sort of deficit would be expected if
non-olfactory sensory information(thecontext) was not appropri-
ately correlated with olfactory information, that is, a failure of
cross-modal integration. In drawing parallels to the theory, we
suggest that themediodorsal nucleus of thethalamus corresponds
to the sensory integrator, correlating input from olfactory and
non-olfactorysourcesfor processinginthecontrolledassociator or
comparator and encoder.
Inconclusion, studiesinvolvinganimalshaveidentifiedseveral
brain areas involved in olfactory learning and memory. These
includethepiriformcortex, prefrontal cortex, mediodorsal nucleus
of thalamus, and the olfactory bulb. All of these structures dem-
onstrateplasticity, suggestingtheubiquity of learningphenomena
inolfactory brainstructures. Finally, atentativecasecanbemade
for correspondences betweenthemodular components of thethe-
ory and particular brain structures: the piriformcortex with the
olfactory processing module, the prefrontal cortex with the con-
trolled associator, and the mediodorsal nucleus of the thalamus
with thesensory integrator.
Neuropsychological Data
Twotypesof predictioncanbemadeabout thehumanolfactory
neuropsychological data. Thefirst derivesfromthetheoryandcan
be succinctly stated. Any interruption in the flow of information
between modules should result in deficits in odor-quality percep-
tionas measured by discrimination and identificationwithout
losses in detectability or sensitivity. (One should note that more
elaborate predictions could be derived but that experimental in-
vestigations to date are relatively blunt.) The second type of
prediction derives from the animal literature discussed above,
namely that similar brain regions should also feature in human
olfaction. Wedeal with this latter issuefirst.
355
A MNEMONIC THEORY OF ODOR PERCEPTION
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In animals, lesions of prefrontal cortex, piriform cortex, and
mediodorsal nucleus of the thalamus impair odor discrimination.
In humans, several conditions affecting similar areas also impair
olfactoryfunction. Theseincludeaging, Alzheimersdisease, Kor-
sakoffssyndrome, temporal lobectomy, focal lesionstoprefrontal
and certain temporal lobe areas (for a review, see Mair et al.,
1995), and Parkinsons disease (Mesholam, Moberg, Mahr, &
Doty, 1998). Neurological damageinagingmayoccur primarilyin
frontal regions (Gabrieli, 1998) as well as in other cortical and
subcortical areas. Alzheimers disease may initially damage me-
dial temporal lobestructuresbeforeextendingtoother areas(Gab-
rieli, 1998). Korsakoffs syndrome especially involves lesions to
thalamicandlimbicstructuresaswell asother areas(Lezak, 1995).
Focal lesionsareself explanatory. Thusall theseconditionsaffect
areas involved in olfaction: aging affects frontal structures, Alz-
heimers affects piriform cortex in the medial temporal lobe,
Korsakoffs affects the thalamus (and possibly medial temporal
lobes), and focal lesions affect frontal or medial temporal lobes.
Finally, for Parkinsons disease, the role of its affected brain
structures aremoredifficult to directly link to olfactory function
anddeficitsheremay occur throughdifficulty inintentional sniff-
ing (seeBarz et al., 1997, for an alternativeaccount). Overall, it
appears that brain structures important for olfaction in rats and
monkeys arealso important for human olfactory perception.
Withinthepresent theory, lesions inthethreemainbrainareas
discussedabovearepredictedtosparedetectionandsensitivitybut
impair perception of odor quality as indicated, for example, by
reduced odor discriminability or identification. Beforeexamining
thedatait isimportant toexcludeapparent deficitsthat arisefrom
two sources. The first, and most obvious, is reduced sensitivity
fromdamageat theperipheral receptor level (seeVarney, 1988).
Thesecond and moresubtlesourceis an inability to performthe
experimental task. This latter concern is very real, becausemany
disorders of olfaction are associated with impaired explicit-
memory function (see Commentary on Assumption 3). Most of
thestudies discussedheretest for sensitivity changes by compar-
ing olfactory detection thresholds in brain-damaged and normal
participants. However, only a few studies have checked for
generalized-task-performance deficits, and we give these studies
proportionally moreweight.
Agingundoubtedly increases olfactory thresholds; older partic-
ipants (50years or older) typically showlower sensitivity thando
younger participants(e.g., Murphy, 1993; Schiffman, 1993). Older
participantsalsoexhibitreducedsuprathresholddiscriminationand
identification when compared with younger participants (Cain et
al., 1995; Doty, 1992). This is probably caused both by reduced
sensitivity and by damage to frontal regions. For Alzheimers
disease, somestudies(e.g., Doty, Reyes, &Gregor, 1987; Morgan,
Nordin, & Murphy, 1995) have identified reduced sensitivity,
whereas others have not (e.g., Kareken et al., 2001; Koss,
Weiffenbach, Haxby, & Friedland, 1988; Rezek, 1987). However,
all studies that have used odor-identification tasks have found
large deficits in such patients, even when nonverbal (picture-
based) procedures wereused. Morerecently, apositron emission
tomography study revealed significant differences in activity be-
tweenthepiriformcortexof Alzheimer andelderlycontrolsduring
odor identification(Karekenet al., 2001), addingfurther weight to
the argument that impairments arise primarily from damage to
olfactory cortex in themedial temporal lobe.
Some studies have revealed reduced sensitivity in Korsakoff
patients (e.g., P. B. J ones, Butters, Moskowitz, & Montgomery,
1978; Potter & Butters, 1980), but others have not (e.g., Mair,
Capra, McEntree, &Engen, 1980). However, inall of thesestudies
patientsdemonstratedreduceddiscriminability. ThestudybyMair
et al. (1980) is of particular interest becauseit also controlledfor
more generalized memory deficits. In this study normal controls
and Korsakoff patients performed three short-term recognition
tests, each including several retention intervals. One test used
odors, one used visual stimuli (faces), and one used auditory
stimuli.
Intheodor test, at thestart of atrial thefirst odor waspresented,
andasecondodor followedafter avariabledelay; thetask was to
judgewhether this was thesameor different fromthefirst odor.
When different fromthe first, this second odor could be either
similar or dissimilar to the first. There were two main findings.
First, participants in the Korsakoff group were uniformly poorer
than control participants at all time intervals on the odor test
moreso for similar than for dissimilar odor pairs.
Second, onthevisual andauditory tests, Korsakoff patientsand
controlsperformedat comparablelevelswhenthecomparisonwas
immediate. However, performance of the Korsakoff group
dropped markedly as the retention interval increased, whereas
performanceof thecontrol groupwasunaffectedover therangeof
intervals tested. Theseresults imply that damageto thethalamus
(andpossiblypiriformcortexfromdamagetothemedial temporal
lobes) adversely affects discriminationconsistent with the
present theory. They also suggest that memory and perception
cannot bedissociatedas easily for odor perceptionas they canbe
for vision and audition.
Theeffects of unilateral andbilateral temporal lobectomy have
also beenstudied. H.M., who receivedbilateral surgical resection
of the medial temporal lobe (Eichenbaum, Morton, Potter, &
Corkin, 1983), showed broadly normal sensitivity on a range of
testsbut performedat chancelevelswhenidentifyingwhether two
odorswerethesameor different andinamatching-to-sampletask.
Thesedeficitsappear tobelimitedtoolfaction, inthat H.M. could
discriminate objects visually and by touch and identify them
(Eichenbaumet al., 1983). BecauseH.M. lost sizableparts of his
piriformcortex during his resection, thesedeficits may beattrib-
utabletoalossof theolfactory processingmodule, insofar asit is
located there.
A further investigation of temporal lobectomy patients was
undertaken by Eskenazi et al. (1983). In Eskenazi et al.s study
patients with unilateral lobectomies were compared with normal
controls. As with H.M., temporal lobectomy was associated with
significantly impaireddiscriminationandidentificationbut inthis
case with some retained capacity, a probable consequence of
having one intact temporal lobe. There were no differences in
performance between participants with left or right temporal ab-
lations. Oneshould notethat wehavenot discussed hemispheric
differences inolfactory informationprocessing, becausethefind-
ingstodateareinconsistent (seeBrand, Millot, & Henquell, 2001)
and differences are small (e.g., Herz, McCall, & Cahill, 1999;
Homewood & Stevenson, 2001).
Damage to prefrontal areas also produces deficits in discrimi-
nation, as reported fromat least two studies. Potter and Butters
(1980) testedprefrontal lesionedparticipants, together withseveral
comparisongroups. Thelatter was composedof 1thalamic lesion
356
STEVENSON AND BOAKES
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patient, a Korsakoff group, brain damaged controls, and normal
controls. SensitivitytestingrevealedsomedeficitsintheKorsakoff
groupandenhancedsensitivityintheprefrontal groupbut noother
difference between groups. All participants were given both a
graded (easy to hard) hue-discrimination test and a graded odor-
discrimination test that was matched for difficulty with the hue
test. Hue discrimination was excellent in all groups, with only a
slight deficit being observed in theKorsakoff patients. However,
olfactory discrimination was at chancelevel for thalamic (except
ontheeasiest test), prefrontal, andKorsakoff groupsbut waswell
abovechancein normal and brain-damaged controls. Thesefind-
ingssuggest that lossof discriminativeability inolfactionisnot a
consequenceof general deficitsinperformanceor sensitivitybut is
morelikely to reflect theinability of participants to perceiveodor
quality following thalamic or prefrontal damage.
Inthesecondstudy of unilateral cortical lesions, J ones-Gotman
and Zatorre(1988) used theUPSIT to assess odor identification.
Theyfounddeficitsingroupswithfrontal andtemporal lesionsbut
not inthosewithparietal lesions, whoseperformancewascompa-
rableto that of normal controls. Therewereno groupdifferences
insensitivity. Identificationwastypicallyreducedbyabout 20%in
thefrontal and temporal groups. Therelatively small sizeof this
loss, when compared with H.M.s total loss, is probably aconse-
quenceof theunilateral natureof theselesions.
Two conclusions can bedrawn regarding thepredictions made
at the start of this section. First, broadly similar brain regions
appear to participate in olfactory information processing in hu-
mansandanimals. Second, damagetoany of thesestructures, and
by implication their proposed correlates in the theory, typically
results in a loss of odor-quality perception (discrimination and
identification), often without affecting detection (sensitivity and
intensity). Theneuropsychological dataalso suggest threefurther
conclusions pertinent to thetheory:
1. Disorders of odor-quality perception(discriminationand
identification) are typically comorbid with disorders of
explicit memory (seeCommentary on Assumption 3 for
implications).
2. Deficits in the perception of odor quality are not easily
dissociated from deficits in odor memory (this is in
markedcontrasttovisionandauditionandagainsuggests
the reliance of olfactory information processing on
memory).
3. Theonly dissociationto emerge(apartial oneat that) is
between theperception of odor quality and detectability
(seeCommentary on Assumption 2 for implications; but
seeWest & Doty, 1995, for acontrary view).
Discussion
Inthisarticlewepresent atheoryof odor-qualityperceptionthat
we believe to be more consistent with the various domains of
recent olfactory researchthanthestimulus-problemapproachthat
has drivenpsychological researchfor muchof thelast 100years.
Thenatureof thetheory and theevidencefor it arediscussed in
earlier parts of the article and we now turn to a more general
theme, namely, theimplications that thetheory has for thewidely
held view that olfactory perception differs in some fundamental
ways fromtheother exteroceptivesenses.
Emphasis ontheuniqueaspects of olfactionhas beencommon
in recent reviews of research on psychological aspects of odors
(e.g., Herz & Engen, 1996; Richardson & Zucco, 1989; Schab,
1991). Wefeel that this is wholly justified and that threefurther
implications fromthe theory add to this conclusion. In total, six
features of olfaction appear to set it apart fromtheother senses:
1. Olfaction is primarily a synthetic sense rather than an
analytic sense.
2. Olfaction does not appear to allowimagery.
3. Odor perception relies moreheavily on experiencethan
do other senses.
4. Theproperties of olfactory memory differ inmany ways
fromthoseof other memory systems.
5. The relationship between language and olfaction is far
moreconstrained than in theother senses.
6. Olfaction has several unusual neuroanatomical features.
Becausethelast threeitems inthis list haveseenfairly extensive
discussion elsewhere (see Herz & Engen, 1996; Richardson &
Zucco, 1989; Schab, 1991), we briefly examine the first three,
which arethosederived fromour theory.
1. Olfaction as a Synthetic Sense
Both vision and audition are characterized by the ability to
analyzethecomponent features of acomplex stimulus, afacility
thatimproveswithpracticeinbothmodalities(e.g., Gibson, 1953).
Olfactionisdifferent fromthisintworespects. First, theinforma-
tion needed to distinguish between the components of an odor
mixturemay not beavailable, becauseof thenatureof olfactory-
information processing. In contrast, the visual system, for exam-
ple, contains a wide variety of cells in the lateral geniculate
nucleusandstriatecortexthat aredifferentiallysensitivetoalarge
range of specific features in the visual world (e.g., Hubel &
Wiesel, 1959). Todate, thereappearsnoobviousanalogy tothese
typeof cells inolfaction, andevenif they exist, their output does
not appear accessibleto consciousness in thesameway as visual
information. Thisisbecauseintheolfactorysystemtherearestrict
limits on the number of stimuli that can be identified in an odor
mixture (see Commentary on Assumption 4). Presumably, if fea-
ture information were accessible, such limits would not be in
evidence.
A secondandrelateddifferenceconcernstheimpactof expertise
on feature detection. In the most careful study of this issue,
Livermore and Laing (1996) observed that experts with many
yearsexperienceinperfumeandflavor designwerenobetter than
novicesinidentifyingthecomponent partsof odor mixtures(con-
trast this for example with visual feature detection, which mark-
edly improves with practice; see, e.g., Myles-Worsley, J ohnston,
& Simons, 1988). This suggests that real physical constraints are
imposedonfeaturedetectioninolfactioninawaynot encountered
in vision and audition.
357
A MNEMONIC THEORY OF ODOR PERCEPTION
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2. Absence of Imagery
Many peoplereport theability to imaginecomplex sounds and
visual images in the absence of external visual and auditory
stimulation (e.g., Baddeley & Andrade, 2000; Dadds, Bovbjerg,
Redd, & Cutmore, 1997; Richardson, 1999). As reviewedearlier,
evidence for imagery in olfaction is weak, and the reason why
olfactionshouldlack this ability, whencomparedwithvisionand
audition, may offer further insights into olfactory processing and
its differences fromtheseother senses.
Thetheory suggests that olfactory stimulationresults inpattern
matchingintheprocessingmodule, withactivatedpatterns repre-
sentingthequalitiesthat areperceived. Thestudyof odor learning,
particularlytastesmell synesthesia, suggeststhat whenanengram
inthestoreisactivatedinthisway, weexperiencethepresenceof
asensoryqualitythat hasnophysical basisinrealitythepercep-
tion of sweetness in this case. This may suggest that odor
imagery is not commonly experienced because the systemis not
equipped to tell apart image fromthe product of real physical
stimulation, injustthesamewaythatweareunabletotell apartthe
real from the learned components of odor quality. Thus the
absence of odor imagery may be an indirect consequence of the
systems lifelongdependenceonlearningto shapeour perception
of odors and theconsequent dissociation between perception and
stimulation.
3. Experience and Olfactory Perception
Although experience is undoubtedly a crucial factor in the
development of both thevisual and auditory system(e.g., Blake-
more& Cooper, 1970; Werker & Tees, 1992), twoaspects of this
process appear to distinguish it fromexperiential development in
olfaction. Thefirst is thesheer lengthof timetakento buildupa
reservoir of olfactoryexperienceandknowledge. Thisprocessmay
extend long into adolescence and even early adulthood (e.g., De
Wijk & Cain, 1994a, 1994b), because odor-identification ability
progressively improvesover thistimeperiod(seeCommentary on
Assumption 1). For vision and audition, major developmental
changesarenearlycompleteby1year (e.g., object discrimination,
visual acuity, color anddepthperception, hearingthresholds), and
if spoken-languagecomprehension is included, thesechanges are
completeby 5 or 6 years.
A second unique developmental characteristic, and one that is
more speculative, is the anatomical consequences of experience.
Exposure to elements in the visual world (horizontal lines for
example) iscrucial for correspondingneural development, aslong
as this occurs within a critical period. We argue that the neural
apparatusfor odor learning(andhenceperception) ispresent from
birth and is not subject to any form of critical period. This
suggestionissupportedbythefollowingevidence. First, babiesare
clearly capable of olfactory learning froman early age, in that
breast-fedinfants canreadily discriminatebetweentheir mothers
smell andthatof another mother, unlikebottle-fedbabies(Cernoch
& Porter, 1985). The presumption here is that exposure to the
mothers skin during breast feeding provides thenecessary expo-
surefor infants to learn distinctions in odor quality. Second, this
ability to learn odor discriminations continues into adulthood, as
indicatedbycontinuedgainsinodor identificationwithageandby
the ability of participants in their 20s and 30s to acquire odor
qualities in the learning studies reported here. Thus, although
experience may be a necessary adjunct for the development of
vision and audition, we argue that experience is odor-quality
perception.
A final point that needs tobemadeconcerns innateresponding
to odors. Although in humans there is currently no compelling
evidenceof innateresponding, theanimal literaturedoesprovidea
limitednumber of examples. Oneespecially interestingoneis the
fear shown to cat odor by rats (Dielenberg & McGregor, 2001).
Thisresponse, whichappearstobewhollyinnate, wouldappear to
run against the experiential arguments advanced in this article.
Likewise, the finding that connections fromthe glomeruli to the
piriformcortex are more specific than once thought (see Neuro-
anatomical Basis of the Theory) might also be taken to imply
direct stimulusresponserelationships, apparently consistent with
innaterather thanlearnedresponses(e.g., Barinaga, 2001). Clearly
innate responding exists and there will be instances in which
hard-wired responses, especially to predator odors, offer an im-
portant selectiveadvantage. Nonetheless, weargue, first, that such
responses are exceptions and, second, that just like a computer,
fixedhardwaredoesnot havetoimply fixedfunction. Learningas
anintegral part of odor perceptionappears to bethenorminboth
humansandanimals, becausetheflexibility thisaffordsindealing
with novel stimuli is both complementary to any innateresponse
and probably, in thefinal analysis, moreimportant.
Conclusion
Thisarticlepresentsanewpsychological theoryof odor-quality
perception. According to the mnemonic theory, stimulus input
fromtheglomerular layer of theolfactory bulb is compared with
existing olfactory engrams in along-termsensory store, possibly
located in the piriformcortex. The theory provides a framework
for understandingavariety of experimental results that havehith-
erto remained disparate and unexplained. In addition, it aligns
psychological research moreclosely with recent developments in
neuroanatomy, neurophysiology, andmolecular biology. Notably,
research in these fields has either explicitly favored this sort of
model or at least strongly impliedit. Finally, our hopeis that the
mnemonic theory will provideaframework for revitalizing work
on odor-quality perception. Odors forman important part of hu-
man subjective experience, and yet the effort to understand this
experiencehaslanguishedbecausethestimulus-problemapproach
has proved inadequate.
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Received J une6, 2001
Revision received J une13, 2002
Accepted J une16, 2002
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