Advanced Review

Learning and cognition in insects

Martin Giurfa1,2
Insects possess small brains but exhibit sophisticated behavioral performances.
Recent works have reported the existence of unsuspected cognitive capabilities
in various insect species, which go beyond the traditional studied framework of
simple associative learning. In this study, I focus on capabilities such as attention,
social learning, individual recognition, concept learning, and metacognition, and
discuss their presence and mechanistic bases in insects. I analyze whether these
behaviors can be explained on the basis of elemental associative learning or, on the
contrary, require higher-order explanations. In doing this, I highlight experimental
challenges and suggest future directions for investigating the neurobiology of
higher-order learning in insects, with the goal of uncovering l architectures
underlying cognitive processing. 2015 John Wiley & Sons, Ltd.
How to cite this article:

WIREs Cogn Sci 2015. doi: 10.1002/wcs.1348

INTRODUCTION

nsects have historically fascinated biologists

because they allow accessing the mechanisms
and the organization of behavior with different levels
of complexity. The fact that insects possess small
nervous systems, with a reduced number of neurons,
does not constitute a limitation for the production of
sophisticated, complex behaviors.1,2 Besides, stereotyped, genetically encoded behaviors, insects exhibit a
remarkable behavioral plasticity as numerous species
learn and memorize different sorts of sensory cues
as predictors of reward37 or punishment812 and
form memories of such experiences that can be
retrieved at different times after learning, from the
short-term to the long-term range. Not surprisingly,
therefore, species such as the fruit fly Drosophila
melanogaster9,13,14 and the honey bee Apis mellifera5,15 have become inspirational models for the
study of memory. The neural circuits underlying such
capabilities are only simple in appearance and exhibit
an exquisite architecture.16 The delusory simplicity
of the insect nervous system was acknowledged by
Santiago Ramn y Cajal, neuroscientist and Nobel
Correspondence

to: martin.giurfa@univ-tlse3.fr

1 Centre

de Recherches sur la Cognition Animale, Universit de

Toulouse (UPS), Toulouse, France

2 Centre

de Recherches sur la Cognition Animale, Centre National

de la Recherche Scientifique (CNRS), Toulouse, France
Conflict of interest: The author has declared no conflicts of interests
for this article.

laureate, who together with his student Domingo

Snchez, expressed well the fascination that insect
nervous systems exert for neurobiologists interested
in the mechanisms of behavior17 :
Insects possess a nervous system that is incredibly
complex and differentiated, and whose fineness attains
ultramicroscopic levels. Comparing the visual and
cerebroid ganglia of a bee or a dragonfly with those
of a fish or an amphibian yields an extraordinary surprise. The excellence of the psychic machinery does
not increase with zoological hierarchy; on the contrary, one realizes that in fishes and amphibians, the
nervous centers have suffered an unexpected simplification. Certainly, the grey substance has considerably
increased in mass, but when one compares its structure with that of the brain of Apidaea or Libellulidae,b
it appears as excessively coarse and rudimentary. It
is like pretending to match the rough merit of a wall
clock with that of a pocket watch, a marvel of fineness,
delicacy and precision. As usually, the genius of life
shines more in the construction of smaller than larger
master piecesc

Most of the research on insect learning and

memory has focused on simple forms of associative
learning such as Pavlovian and operant conditioning.
In the former, animals learn an association between
a conditioned and an unconditioned, biologically
relevant stimulus.18 In the latter, they learn to associate a behavioral action with the reinforcement
resulting from that action.19 In both cases, the appeal
of insects resides in the possibility of tracing these

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(a)
Toothpick with
sucrose
Harnessed
bee

CS

US

Odor delivering setup

(b)

Yaw torque signal

Laser diode

Computer

Light
Torque source
meter

Color filter
Light
guides

Electronic
motor

Diffusor
Arena position

FIGURE 1 | (a) Pavlovian olfactory conditioning of the proboscis extension response (PER) in restrained honeybees. Left panel: an individual bee
is immobilized in a metal tube so that only the antennae and mouth parts (the proboscis) are free to move. The bee is set in front of an odorant
stimulation setup which is controlled by a computer and which sends a constant ow of clean air to the bee. The air ow can be rerouted through
cartridges presenting chemicals used for olfactory stimulation (conditioned stimuli or CS). Sucrose solution (unconditioned stimulus or US) is delivered
by a toothpick to the antennae and to the proboscis. Right panel: After conditioning, the odor CS, which initially did not evoke any response, triggers
the PER. (b) Operant visual conditioning of a tethered fruit y (courtesy of B. Brembs). Left panel: A Drosophila is ying stationary in a cylindrical
arena. The ys tendency to perform left or right turns (yaw torque) is measured continuously and fed into a computer, which controls arena rotation.
On the screen four landmarks, two Ts and two inverted Ts, are displayed in order to provide a referential frame for ight direction choice. A heat
beam focused on the ys thorax is used as an aversive reinforcer. The reinforcer is switched on whenever the y ies toward a prohibitive direction.
The y controls therefore reinforcer delivery by means of its ight direction. Right panel: Detail of a tethered y in suspended ight within the ight
simulator.

simple associative links to specific neurons and circuitries. Yet, the last decade has generated a wealth
of novel research on insect learning and memory
which has overcome the classical framework of simple forms of associative learning to focus on more
elaborate cognitive capabilities.1,2 This includes work
on attention-like processes in fruit flies and honey
bees,20,21 observational learning in a social context
in bees, crickets and flies,2227 individual recognition
in wasps,2830 categorization,31 concept learning3234
and meta-cognitive like processes in bees.35 These
reports yield new light on the cognitive richness of
insect behavior, which appears to transcend basic
Pavlovian and operant learning. Here, I focus on a
selection of recent findings on learning and cognition
in insects and discuss whether behaviors that appear
particularly complex can be explained on the basis

of elemental associative learning or on the contrary,

require explanations that go beyond this level.

PROTOCOLS FOR THE STUDY OF

ELEMENTAL ASSOCIATIVE LEARNING
IN INSECTS
Pavlovian Conditioning
Multiple cases of Pavlovian conditioning have been
described and studied in insects. For instance, in the
honey bee Apis mellifera, olfactory conditioning of the
proboscis extension response (PER) has been repeatedly used for the study of elemental classical conditioning and its neural substrates.3638 Individually
harnessed hungry bees (Figure 1(a)) respond to a stimulation of their antennae with sucrose solution (the

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WIREs Cognitive Science

Learning and insect cognition

unconditioned stimulus [US]) with an extension of

their proboscis (PER). If a neutral odor (the conditioned stimulus [CS]) is forward-paired with sucrose,
the bees learn an elemental association between odor
and sucrose reward, so that they exhibit conditioned PER to later presentations of the odor alone
(Figure 1(a)). The association built is Pavlovian and,
depending on the number of trials, interstimulus interval, intertrial interval, and so on, can be consolidated
in short-, mid-, or long-term memories.5,37 In particular, memory induced by a single-trial conditioning
(weak training) decays over time, is sensitive to amnestic treatments, and is independent of translation and
transcription.5 Repetition of trials (at least three trials with a 10-min intertrial interval) induces a stable, long-lasting memory (>7 days) that is insensitive
to amnestic treatments and requires translation and
transcription.5
In a straightforward reproduction of Pavlovs
conditioning of dog salivation, olfactory conditioning
of salivation was shown in cockroaches Periplaneta
americana.39 In this insect, salivary neurons that
control salivation exhibit increased responses to an
odor after conditioning trials in which the odor was
paired with sucrose solution. Saliva is released into
the cockroachs oral cavity via the salivary duct. In
prepared animals, collecting saliva from this duct was
possible via a capillary so that salivation activity could
be quantified. In this way, conditioning of salivation
was demonstrated by pairing one odor with sucrose
and a different odor with the absence of sucrose;
the former, but not the latter, induced a conditioned
increase of salivation.39
Classical conditioning has also been intensively
studied in the fruit fly Drosophila melanogaster. Flies
can easily be trained to associate an odor (the CS)
with an aversive electric shock (the US). The typical
procedure consists in training groups of flies alternatively presented with two different odors, one paired
with an electric shock (CS+), and another nonpaired
with the shock (CS).40 Retention is measured in a
T-maze where conditioned flies must choose between
the CS+ and the CS. As in honey bees (see above),
stronger and longer-lasting memory is generated when
training is repeated (usually 510 times) and training cycles are spaced by 15 min (spaced training). In
this case, a memory that may last for several days and
that depends on protein synthesis is formed. If training cycles are spaced by 30 seconds (massed training),
the memory created is independent on protein synthesis. By increasing the time between training and testing
and using disruptive treatments, it has been possible
to measure and characterize different memory phases
such as short, mid-, or long-term memories.9,12

Operant Conditioning
Operant learning underlies the extensive studies on
visual learning and perception in bees performed in the
last 100 years, since the pioneer work of Nobel-prize
winner Karl von Frisch.41 A free-flying bee, identified by a color spot on the thorax or abdomen,
can be trained to choose a visual target associated
with the appetitive reinforcement of sucrose solution.
The associations built in these context can be either
operant, classical or both, i.e., they may link the
response of the animal (e.g., landing) and the reinforcement, the visual stimuli and the reinforcement,
or both. The experimental framework is nevertheless mainly operant as the bee freely decides where
and when to land to obtain the sucrose. The bees
behavior is thus determinant for accessing or not the
reinforcement.
The fruit fly has also played a pivotal role
for the study of operant learning. In this case, a
Drosophila is suspended from the thorax in the middle
of a cylindrical arena that allows the presentation
of visual landmarks (Figure 1(b)).42 The tethered
fly flies stationary and if some of these landmarks
are paired with the aversive reinforcement of an
unpleasant heat beam pointed on the thorax, the fly
learns to fly toward a safe direction, avoiding the
dangerous-landmark directions42,43 (Figure 1(b)). The
fly learns to control reinforcement delivery as its flight
manoeuvres determine the switching-off of the heat
beam if the appropriate flight directions are chosen,43
thus constituting a case of operant learning. Classical
associations can also be established between the visual
landmarks displayed on the cylinder wall and the
reinforcer.44 In another operant protocol, the heat
box, a Drosophila fly has to learn to avoid the half
of a small dark chamber that is heated every time
the fly walks in.45,46 As soon as the animal leaves
the punished half, the chamber temperature reverts
to normal. Flies learn to restrict their movements to
one-half of the chamber, even in the absence of heating
punishment. This memory is still detectable even if the
fly is taken out of the chamber and then tested 2 h
later.46
In the blood-sucking insect Rhodnius prolixus,
PER is induced by thermal stimulation close to that
of the skin surface of potential vertebrate hosts (35 ).
Operant inhibition of PER was shown by making
a thermal shock contingent with PER.47 Bugs that
responded with PER to a thermal stimulation of 35 C
received a heat shock on the extended proboscis by
increasing the temperature to 50 C; in this way, bugs
stopped responding with PER to thermal stimulation and retained the operant association up to 72 h
later.47

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A CHANGE OF PARADIGMS
In the nineties, research on insect learning and memory experienced a significant change; beyond simple associative learning, based on protocols such as
those described above, some researchers started focusing on the possibility that insects exhibit higher-order
forms of learning. The cognitive revolution, which
had already impacted long before the field of animal
learning48 and introduced the view that animals are
goal-seeking agents that acquire, store, retrieve, and
internally process information at many levels of cognitive complexity, reached with a certain delay the
field of insect learning and memory. A change in conceptual approaches followed, not only because insects
were not anymore considered as miniaturized robots
exhibiting reduced plasticity, but because novel questions focusing on cognitive capacities, whose study
had remained the exclusive domain of vertebrates,
started to be raised and answered experimentally.
What follows is a series of examples which do not
pretend to be integral but rather illustrative of these
questions.

ATTENTIONAL PROCESSES IN
INSECT PERCEPTION
Several reports have indicated that attentional processes, similar to those described in vertebrates, can
also be identified in insects. Studies on bumblebee
and honey bee color learning49,50 suggested that attentional processes may dramatically affect discrimination capabilities and that the key issue is how the
bees learn the visual task.51 The role of attention in
visual object recognition has been explicitly studied in
honey bees trained to choose a colored disc (target)
among a varying number of differently colored discs
(distracters).21 Accuracy and decision time were measured as a function of distracter number and color. For
all color combinations, decision time increased and
accuracy decreased with increasing distracter number,
whereas performance improved when more targets
were present. Similar results are found in studies on
visual attention in which primates inspect visual stimuli sequentially. This convergence suggests that serial
visual attention is common to mammals and bees.21
Visual attention has also been studied in fruit
flies.20 A tethered fly flying stationary within a cylindrical arena (similar to that in Figure 1(b)) and tracking a visual object (a vertical black bar displayed on
the cylinder wall) moving at a constant frequency
around it, exhibits anticipatory behavior consistent
with attention for the bar it tracks. In another work,
competing moving gratings were presented to either

eye of the fly in the cylindrical arena.52 Confronted

with these competing percepts, flies alternated their
flight direction between the right and the left moving
grating, in an attention-like process that suppressed
responses to the nonfollowed grating.52

LEARNING IN A SOCIAL CONTEXT

A social life style is characteristic of many
Hymenopterans (bees, wasps, and ants). Among
them, honey bees have evolved a unique communication behavior, the waggle dance,53 which constitutes
one of the most efficient animal systems known for
information transfer about profitable food sources.
A successful forager performs a stereotyped behavior
within the hive, originally described as a dance,
which conveys information to the receivers about the
direction and distance from the hive of an exploited
food source.5456 Although the behavioral encoding and decoding of these variables have a genetic
basis,53 interindividual learning occurs in the context
of dances. Dancers returning from profitable flowers
deliver regularly during the dance a drop of scented
nectar to the bees following the dance. In this way,
followers learn the association between odor and
scent characteristic of the flower exploited by the
dancer. Odors learned in this way can afterward drive
appetitive responses to food in bees that had a priori
no contact with flowers.57,58
Recent studies have also indicated that insects
copy the behavior of conspecifics in contexts as diverse
as foraging, in the case of bumblebees,23,24,59 mate
choice, in the case of flies60 and predator avoidance in the case of crickets.27 Bumblebees, e.g.,
learn foraging preferences from other bumblebees by
observing their choices of visual rewarded targets
(Figure 2(a)). They land on unknown flowers if other
bees are already present at them.24 This behavior is
exhibited even when nave bees are separated from
experienced foragers by a transparent screen such
that they can neither sample the flowers by themselves nor interact with their foraging conspecifics.23
Similarly, nave bumblebees abandon an unrewarding
flower species and switch to a more rewarding alternative more quickly when accompanied by experienced
foragers.25
Another example of learning in a social context is provided by the fruit fly in a mating and an
oviposition context.26,60 Two male phenotypes were
artificially generated by dusting individuals with green
or pink powder. In this way, females could differentiate between these two types of male.60 An observer
female was placed in a glass tube from which it
could see the interaction between a painted male and

2015 John Wiley & Sons, Ltd.

(a)

Percentage of observer bees choosing

the flower occupied by a demonstrator

WIREs Cognitive Science

Learning and insect cognition

80

(b)

***

Demonstrator (CS1)

60

40

***

Feeder (US)

20

Demonstrator (CS1)

0
First trial

(c)

Observer

1st phase

Subsequent choice
of alternative feeder

Observer

2nd phase

CS1
CS2

Novel feeder
Color/odor (CS2)

US

FIGURE 2 | Social learning in bumblebeesan elemental account. Percentage of choices by observer bees of a feeder occupied by a
demonstrator bee. The arena contained eight feeders, four blue, and four yellow. The demonstrator was placed on one feeder type, yellow or blue,
and the observer released in the arena. Right bar: Choices of the feeder occupied by a demonstrator in the rst trial, when both feeder types were
unfamiliar to observers. Left Bar: Choices of the alternative feeder type in subsequent trials when it was occupied by a demonstrator. The dashed line
corresponds to a random choice in a situation where eight feeders were available. Asterisks correspond to P < 0.01. (Reprinted with permission from
Ref 24. Copyright 2005 Cell Press). (b) Possible associations established by bumblebees during social learning in a foraging context. During direct
interactions with demonstrators, observers experience nectar reward (US; green arrow) and associate demonstrators (conditioned stimulus 1 or CS1)
with the US (red arrow); if demonstrators come to choose a novel feeder (here with a different color), observers will also land on the novel occupied
feeder and will associate the physical properties of the owers that demonstrators now exploit (CS2) with the demonstrators themselves (CS1; red
arrow). The process postulated corresponds to a case of second-order conditioning. (c) Nature of associations established during the two phases of a
second-order conditioning process.

another female. In one case, the male which was, say

green, copulated with the demonstrator female, and
in other case, the other male which was, say pink,
did not copulate because it was paired with nonreceptive female. After this double demonstration, the
observer female was presented with two new males,
one pink and the other green. Observer females preferably mated with males of the color that was associated with a successful copulation, over males of the
color which were associated with unsuccessful copulative attempts. This effect disappeared when observer
females were impeded to observe directly the other
flies during their interaction.60 Comparable results
were found in an oviposition context26 : the choice
of oviposition sites by Drosophila females is influenced by experienced demonstrator females, which
have been conditioned to avoid one of two equally
rewarding media. Surprisingly, oviposition site preference was socially transmitted from demonstrators to

observers even when they interacted in a cage with

only unflavored, pure agar medium, and even when
the observer flies had previous personal experience
with both rewarding media.26
Observing and then deciding own actions are,
therefore, capabilities that are also present in small
brains. Yet, as fascinating as they may appear, none
of these works provide insights into the mechanisms
responsible for these behaviors. This is particularly
surprising in the case of Drosophila, where the availability of neurogenetic tools and of many mutant lines
would allow to address the question of the neural
structures and circuits involved in social learning (as
compared, e.g., with those mediating elemental Pavlovian learning). Here, again, a change in paradigm
is still pending: researchers interested in Drosophila
social behavior have not yet taken the step to move
into neural analyses but this transition will probably
not take long.

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A fundamental exercise is to determine whether

elemental accounts, based on simple associative links,
can explain the insect behavior in these different contexts. This appears plausible in most, if not all, cases
considered. The case of bumblebee social learning
described above, for instance, can be interpreted in
terms of an elemental form of associative learning
called second-order conditioning,18 which involves
two connected associations (Figure 2(b) and (c)). In
this scenario, an animal first learns an association
between a CS and an US. It then experiences a pairing between a new conditioned stimulus CS2 and CS1
so that CS2 becomes meaningful through its association with CS1, and indirectly with the US (Figure 2(c)).
With this in mind, one can propose that nave bumblebees first associate the presence of a conspecific
(CS1) with reward (US) simply by foraging close to
experienced foragers (Figure 2(b)). Subsequently, the
observation of a conspecific landing on a given color
(CS2) may allow establishing an association between
color (CS2) and conspecific (CS1).25 The hypothesis
of connected elemental links is supported by the fact
that honey bees and fruit flies can learn such 2nd -order
associations while searching for food. They learn to
connect both two odors (Odor 1 + Sucrose Reward;
Odor 2 + Odor 136,61 ; and one odor and one color.62
The hypothesis of second-order conditioning as
a mechanism for observational learning has been
recently shown in experiments in which bumblebees
learn how to recognize rewarding flower colors by
watching conspecifics from behind a screen.22 Bees
that were previously rewarded with sucrose solution
for joining conspecifics copied their color preferences,
but bees that lacked such experience did not. In a
parallel experiment, bees that associated conspecifics
with a bitter quinine solution actively avoided those
flower colors where others have been seen. These
results thus constrain social learning within a simple
associative framework. Identification of the cues that
are learned and analysis of their processing in the
insect brain are goals for future research.

INDIVIDUAL FACE RECOGNITION

The capacity to recognize the distinctive identity of
individuals has long been dismissed in social insects
because of the cognitive requirements that such performance may impose in colonies with thousands of
individuals. Not all social insects live, however, in huge
overcrowded societies. Small colonies of bumble bees,
wasps and some ant species are based on dominance
hierarchies where individual recognition may be crucial for responding appropriately to a conspecific. In
these cases, individual recognition based on olfactory

cues might well be possible given the high dimensionality of olfactory coding in Hymenoptera.63 For
instance, unrelated queens of the ant Pachycondyla villosa use chemical cues to recognize each other individually, thereby modulating aggression depending on the
degree of familiarity existing between them. This modulation remains in choice experiments in which physical contact, but not odor perception, was prevented,64
thus showing the olfactory nature of the interindividual recognition.
In the visual modality, studies on the paper wasp
Polistes fuscatus showed that individual recognition is
achieved through learning the yellowblack patterns
on the wasp faces (the so-called masks) and/or
abdomens, which act as efficient labels of social
hierarchy.29 Altering facial and/or abdominal color
patterns induced aggression, irrespective of whether
their patterns were made to signal higher or lower
social ranking. These results indicate, therefore, that
individual wasps learn and use these visual features for
inter-individual recognition.30 Recently, a new twist in
this story was introduced by comparing two closely
related wasp species, P. fuscatus and P. metricus,
which differ in their social structure and ability to
recognize wasp faces28 : P. metricus, contrary to P.
fuscatus, nests alone, does not present facial-mask
variability and as a consequence does not exhibit
individual recognition. Individuals of both species
were trained to discriminate images within a small
T-maze in which incorrect choices were punished with
an electric shock delivered though an electrified floor.
Images included photos of different P. fuscatus faces,
different caterpillars, and black and white patterns
such as vertical and horizontal gratings, a cross, and
a concentric ring pattern.28 While P. fuscatus wasps
differentiated among normal P. fuscatus face images
more rapidly and accurately than nonface images or
manipulated faces, P. metricus, was unable to learn
this discrimination. Interestingly, both species learned
to discriminate caterpillar images and abstract pattern
images but in the case of P. fuscatus such learning
yielded lower discrimination when compared with
face discrimination. These data suggest that P. fuscatus
do not use general pattern- or shape-discrimination
abilities, which are also present in P. metricus, to
recognize conspecific faces. Instead, faces appear to be
treated as unique visual inputs by P. fuscatus, resulting
in improved discrimination performances.28 Yet, the
comparison with abstract patterns which were learned
less well than wasp faces to sustain the conclusion
of a specialized face recognition system is debatable:
the patterns chosen (i.e., a cross vs a grating) did
not facilitate visual recognition as they stimulated
common neural detectors (i.e., a vertical orientation

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Learning and insect cognition

detector responding both to the vertical axis of the

cross and to the vertical bars of the grating). This
criticism does not invalidate the conclusion on the
presence of an improved face discrimination in P.
fuscatus compared with P. metricus.
Polistes fuscatus is sensitive to the specific configuration features defining a facial masks so that scrambling pattern components alters the wasps response.28
Previous experiments with honey bees have shown
that these insects are able to learn feature configurations present in a series of different visual patterns
so that they detect and choose novel stimuli presenting the extracted configuration.65,66 A similar form
of visual configural learning may operate in P. fuscatus wasps, with a particular sensitivity for those
features defining facial pattern configurations. In the
maze experiments, a simple association between the
appropriate configuration and the absence of electric
shock may account for the learning performance of P.
fuscatus wasps. In a natural context, each individual
facial mask would have an unambiguous significance
in terms of its ranking in the social structure (i.e., mask
A individual; mask B individual, etc.) so that
wasps would learn a series of elemental associations
between mask patterns and social ranking. Given the
small size of colonies in which 510 individuals can
coexist, storing several memories, one for each individual, appears plausible. If this were the case, a fundamental research goal would be to characterize the
storage capacity and accuracy of the visual memory in
relation to colony size.

LEARNING ABOUT CONCEPTS

A higher level of complexity is reached when animals
respond in an adaptive manner to novel stimuli that
they have never encountered before and that do not
predict a specific outcome based on the animals past
experience. Such a positive transfer of learning (also
called stimulus transfer) brings us, therefore, to a
domain that differs from that of elemental forms of
learning.67
Concept learning is particularly interesting for
the study of nonelemental learning as it consists of
learning relations between objects rather than the
physical properties (colors, shape, size, etc) of the
objects themselves.68,69 As a consequence, transfer
performances should be able to identify the relationship learned, independently of the physical nature of
the stimuli considered.70,71 Examples of such relations
are same as, different of, above/below of, on the
left/right of, and so on. Extracting such relations
allows transferring a choice to unknown objects that

may differ dramatically in terms of their physical

features but that may fulfill the learned relation.
Various recent reports have indicated that honey
bees learn relational rules of different sort. These
include sameness/difference,32 above/below,33
and the mastering of two rules simultaneously,34
above/below (or left/right) and different of.

Sameness/Difference Concepts
The learning of the concepts of sameness and difference was demonstrated through the protocols of
delayed matching to sample (DMTS) and delayed nonmatching to sample (DNMTS), respectively.32 In the
former, the subject must match its choice to a stimulus that corresponds to a sample previously presented.
As the sample is regularly changed during the training, animals must learn the concept of sameness, i.e.,
always choose what is shown (the sample), independently of what else is shown. In the latter, the subject must choose a stimulus that is explicitly different
from a sample previously presented. As the sample is
regularly changed during the training, animals must
learn the concept of difference, i.e., always choose the
opposite of what is shown (the sample), independently
of what else is shown.
Honey bees foraging in a Y-maze (Figure 3(a))
were trained in a DMTS experiment in which they
were presented with a changing nonrewarded sample (i.e., one of two different color diskscolor
groupor one of two different black-and-white gratings, vertical or horizontalpattern group) at the
entrance of a maze (Figure 3(b)). The bees were
rewarded only if they chose the stimulus identical
to the sample once within the maze. Bees trained
with colors and presented in transfer tests with
black-and-white gratings that they had not experienced before solved the problem and chose the grating identical to the sample at the entrance of the
maze. Similarly, bees trained with the gratings and
tested with colors in transfer tests also solved the
problem and chose the novel color corresponding
to that of the sample grating at the maze entrance
(Figure 3(c)). Transfer was not limited to different
types of visual stimuli (pattern vs color), but could also
operate between drastically different sensory modalities such as olfaction and vision.32 Bees also mastered a DNMTS task, thus showing that they learn
a rule of difference between stimuli as well.32 These
results were the first to document that bees learn rules
relating stimuli in their environment. They were later
verified in experiments showing that bees categorize
visual images based on general features common to
these images72 and in a study showing that the sensory

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Advanced Review

(a)

(b)

Transfer
test

(c)

Transfer tests with patterns

(training with colours)

Transfer tests with colors

(Training with patterns)

100
Preference for vertical
Preference for horizontal

Training
(60 trials)

% correct choices

80

Preference for blue

Preference for yellow

Vertical

Horizontal

60
40
20
0

Pattern
group

Colour
group

Blue

Yellow

Sample

FIGURE 3 | Sameness learning in honey bees. (a) Y-maze used to train bees in a delayed matching-to-sample task. Bees entered into the maze to
collect sugar solution on one of the back walls of the maze. A sample was shown at the entrance before bees accessed the arms of the maze. (b)
Training protocol. A group of bees were trained during 60 trials with black-and-white, vertical and horizontal gratings (Pattern Group); another group
was trained with colours, blue and yellow (Colour Group). After training, both groups were subjected to a transfer test with novel stimuli (patterns for
bees trained with colours, colours for bees trained with patterns). (c) Performance of the Pattern and the Colour Group in the transfer tests. Both
groups chose the novel stimulus corresponding to the sample although they had no experience with such test stimuli. (Reprinted with permission
from Ref 32. Copyright 2001 Nature Publishing Group, Macmillan Publishers Limited).

memory underlying the solving of the DMTS task lasts

for approximately 5 seconds,73 a period that coincides
with the duration of visual and olfactory short-term
memories characterized in simpler forms of associative
learning in honey bees.5

Above/Below Concepts
For many animals that must navigate in complex natural environments, spatial concepts such as right, left,
above, and below are of crucial importance to generate appropriate relational displacements and orientation in their environment. A recent work studied
whether honey bees learn an above/below relationship between visual stimuli and transfer it to novel
stimuli that are perceptually different from those used
during the training.33 Bees were trained to fly into
a Y-maze and choose visual stimuli presented above
or below a horizontal bar. Training followed a differential conditioning procedure in which one spatial
relation (e.g., target above bar) was associated with
sucrose solution whilst the other relation (e.g., target below bar) was associated with quinine solution.
One group of bees was rewarded on the target above
bar relation while another group was rewarded on
the target below bar relation. After completing the
training, bees were subjected to a nonrewarded transfer test in which a novel, discriminable target stimulus
(not used during the training) was presented above or
below the bar. Despite the novelty of the test situation,
which preserved the spatial relationship to the bar
as the single criterion predicting or not the presence

of sucrose reward, bees responded appropriately: if

trained for the above relationship they chose the novel
discriminable stimulus above the bar, and if trained
for the below relationship they chose the novel stimulus below the bar.33 A series of controls showed that
bees were not just averaging a higher frequency of
images either in the upper (if trained or above) or in
the lower (if trained for below) visual field but were
indeed using a relational rule.33
These results showed that bees possess the faculty to extract a conceptual above/below relationship from a set of training stimuli and to transfer
this concept to newly encountered stimuli. This faculty can be useful in a navigational context in which
bees may decide routes based on spatial relationships
between landmarks, which could be generalized to
novel situations.74

Mastering Two Concepts Simultaneously

Processing several concepts simultaneously presupposes an even higher level of cognitive sophistication
than dealing with one concept at a time. In a recent
work,34 honey bees were shown to rapidly master
two abstract concepts simultaneously, one based on
spatial relationships (above/below and right/left), and
another based on the perception of difference.
Bees that learned to classify visual targets
using this dual concept transferred their choices to
unknown stimuli that offered a best match in terms of
dual-concept availability: their components presented
the appropriate spatial relationship and differed from

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WIREs Cognitive Science

Learning and insect cognition

one another. As in the previous study,33 a series of

internal within-subject controls and simulation algorithms allowed researchers to exclude confounding
low-level cues such as the global center of gravity, the
global orientation of the stimuli or the retinotopic
similarity between the rewarded stimuli. These results
thus demonstrated that the small brain of bees can
abstract at least two different concepts from a set
of complex pictures and combine them in a rule for
subsequent choices.34

Concepts That May Not be Concepts

Recent work has argued that that free-flying honeybees learn to solve discrimination problems based
on the acquisition of the concepts of larger than or
smaller than.75 Bees were trained to fly into a Y-maze
to choose either the larger (6x6 cm) or smaller (1x1
cm) stimulus as the correct solution providing sucrose
solution. They subsequently applied the learnt rule to
novel colors and shapes of varying and intermediate
sizes that preserved the trained relationship.
Yet, the experimental design used in this work
presented a problem that precludes a definitive conclusion on concept learning: bees were trained using
6 different stimulus sizes, from 1 1 to 6 6 cm; 15
possible combinations of sizes were presented to the
bees during the training, with one stimulus in the pair
being always larger than the other. Although a given
stimulus size (e.g., 3 3 cm) could be either rewarded
or punished in different foraging bouts depending
on the alternative size with which it was presented
(e.g., 2 2 or 5 5 cm), the two extremes of the scale,
1 1 and 6 6 cm, had a constant association with
reinforcement, i.e., bee trained for larger than had
variable reinforcements in all stimuli except in 6x6
cm which was always rewarded (five times) and in
1 1 cm which was always nonrewarded (five times);
in the case of bees trained for smaller than, 1 1 cm
was always rewarded (five times) and 6 6 cm was
always nonrewarded (five times). The novel transfer
stimuli used to determine whether bees used a rule
were 2.5 2.5 and 4.5 4.5 cm. However, for bees
trained to always choose the smaller stimulus, the
training stimuli that were adjacent to the appropriate
test alternative (2.5 2.5 cm) were 2 2 and 3 3 cm,
which were rewarded in 80 and 60% of their appearances during training; in contrast, the training stimuli
that were adjacent to the inappropriate test alternative
(4.5 4.5 cm) were 4 4 and 5 5 cm. These stimuli
were rewarded in 40 and 20% of their appearances
during training. Thus, it could be possible that in the
transfer tests, bees trained for smaller than chose the
smaller alternative (2.5 2.5 cm) because of its higher

probabilistic association with reward. The same kind

of reasoning could be applied for bees rewarded for
choosing always the larger stimulus.75
In other words, the transfer performance of
bees in these experiments could be explained not
on the basis of a conceptual rule, but just on the
basis of purely associative arguments, i.e., in terms
the probabilistic association of one stimulus class
with reward. As long as this kind of associative
interpretations are not excluded (by establishing, e.g.,
a reinforcement schedule in which all stimuli have
exactly the same probability of being reinforced and
nonreinforced), conclusions on conceptual learning
need to be formulated with caution.

METACOGNITIVE-LIKE PROCESSES
IN HONEY BEES
If cognition can be considered as the ensemble of
faculties that refer to internal representations or
context-dependent memories that reflect these contents, metacognition may be considered as the knowledge of these contents (i.e., the knowing to know).76
Cognitive behavioral biology has focused on
metacognition as a fundamental way to determine
whether animals perform introspective evaluation of
their knowledge before engaging or not in a difficult
task.76 The questions addressed by this research are:
can an animal report on its own degree of confidence
in its behavior, for example by choosing the level of
risk or nonrisk in its responses? Can it show that
it does not know through active research for more
information?
While metacognitive research has shown that
nonhuman vertebrates (mostly primates) selectively
avoid taking difficult tests of memory or perception, collect more information if needed before
taking tests, or gamble more food reward on correct than on incorrect responses in tests of memory
and perception,76,77 a single study has addressed
so far the question of whether an insect may display
metacognitive-like processes.35 Not surprisingly, given
the performances described in the previous section,
the insect chosen was the honey bee.
Bees were trained to solve the above/below
conceptual discrimination (see above), which varied
in difficulty between trials (the images mediating the
relationship were clearly apart or very close to each
other in the vertical plane; Figure 4). Free-flying bees
were rewarded for a correct choice, punished for an
incorrect choice, or could avoid choosing by exiting
the trial (opting out). Bees opted out more often
on difficult trials, and opting out improved their
proportion of successful trials. Bees could also transfer

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wires.wiley.com/cogsci

Advanced Review

(a)

Easy

Difficult

Novel target above

Impossible

Novel target above

Novel target same height

Difficulty tests
with novel targets

Novel target
below

Target below
Punishment
Reward
Target above
Reference bar

0.6

0.4

0.2
1

Exit of decision
chamber
Reference bar
Target
below

Block of 5 trials
(training)

Training
above/below
conceptual rule
30 trials

Punishment

Transfer impossible

Target above
Reward

0.8

Transfer difficult

Novel target below

1.0

Transfer easy

Transfer test
with novel
targets

(b)

Transfer test

Novel target above

Proportion correct choices

Novel target
below

FIGURE 4 | Metacognitive-like processes in honey bees. (a) Experimental schedule. During the training, a horizontal black bar was used as the
reference to dene the above/below relationship. Targets were the same on both sides but variable between the 30 training trials. Reward (2 M
sucrose) or punishment (quinine) was placed in a translucent microcentrifuge tube in the center of the targets. Within a trial, stimulus pairs were
identical except for vertical position relative to the reference bar and relative to the bottom of the chamber. Between trials, targets and positions of
targets and reference bars were varied so that bees could only learn the above/below relation of targets to the references as predictors of reward. In
the example shown, the above relationship was rewarded and the below relationship punished. The transfer tests were unrewarded and used a novel
target not used during the training. In the difculty tests, the easiness of the discrimination was varied by changing the distance between the target
and the horizontal of the reference bar. For easy trials, the target was clearly above or below the reference bar and did not overlap with the reference
bar. For difcult trials, targets partially overlapped with the reference bar. For impossible trials, the center of both targets was in line with that of the
reference bar. (b) Performance of bees. Proportion of correct choices as a function of blocks of ve training trials (training) and performance in
nonrewarded transfer test (red bar). Performance on tests varying in difculty is also shown (green bars). Bees performed better on easy
(83.8 2.5%) than on difcult (52.4 2.5%) or impossible tests (44.5 7%) tests. (Reprinted with permission from Ref 35. Copyright 2013 National
Academy of Sciences).

the concept of opting out to a novel task.35 These

experiments showed, therefore, that bees selectively
avoid difficult tasks when they lack the information
allowing them to solve efficiently the discrimination.
Yet, caution is required when interpreting these
findings as a proof for metacognition as many of the
demonstrations of metacognition in nonhumans can
be explained in terms of associative learning or other
mechanisms that do not require invoking introspection or access to private mental states.77 The authors
of the bee study acknowledged this fact and provided
an alternative a more simple explanation for the bees
performance in associative terms: through training,
difficult stimuli became associated with a high likelihood of punishment because of the high error rate in

these trials; although not itself rewarding, the opt-out

response still would also have a conditioned response
strength because it provides a way to avoid punishment. These assumptions alone are sufficient to predict
that bees will opt out more for hard than easy trials, and that performance should be better in unforced
than in forced hard trials.35 Further experiments conceived to rule-out these associative explanations are
thus necessary to determine whether or not metacognition exists in insects.

CONCLUSION
The present review highlights novel studies on insect
associative learning which in most of the cases had

2015 John Wiley & Sons, Ltd.

WIREs Cognitive Science

Learning and insect cognition

the intention of transcending the traditional framework of research on simple stimulusstimulus (or
behaviorstimulus) associations. They are all inscribed
within a relatively new tendency of appreciating the
cognitive sophistication of the insect brain.1,7882 Such
a tendency is welcome in a field where focus on simple
learning forms may have sometimes overlooked the
enormous richness of insect behavior. Yet, as underlined in this article, not all the feats presented as
highly cognitive are in fact distinct from nonelemental
learning forms. A fundamental goal in conceiving and
interpreting complex insect behavior is therefore, to
critically determine whether basic levels of interpretation are possible and to what extent they account for
plastic insect behavior. Focusing on the neural bases of
insect higher-order learning is certainly a way to avoid
such a caveat as the characterization of neural architectures should constitutes a dispassionate endeavor.
The study of simple learning forms in insects,
both appetitive and aversive, has yield light on how
neural circuits interact to produce plastic behavior
and which functional and structural changes occur at
different stages of these circuits to support elemental

learning and memory formation. As in larger brains,

two basic neural architectural principles of many
invertebrate brains are the existence of specialized
brain structures and circuits, which refer to specific
sensory domains, and of higher-order integration
centres, in which information pertaining to these
different domains converges and is integrated, thus
allowing cross-talking and information transfer. These
characteristics may allow positive transfer from a set
of stimulus to novel ones, even if these belong to
different sensory modalities. This principle appears
crucial for certain tasks such as rule learning. With this
in mind, a qualitative step forward in the study of these
phenomena would be to integrate this knowledge in
an understanding of nonelemental learning forms in
order to answer remaining questions.

NOTES
a
b
c

The large family of bees.

The large family of dragonflies.
Translated by M. Giurfa.

ACKNOWLEDGMENTS
This work was supported by the Institut Universitaire de France, the French National Research Agency
(ANRMINICOG), and the Human Frontier Science Program (HFSP).

REFERENCES
1. Chittka L, Niven J. Are bigger brains better? Curr Biol
2009, 19:R995R1008.
2. Avargus-Weber A, Deisig N, Giurfa M. Visual cognition in social insects. Annu Rev Entomol 2011,
56:423443.
doi:10.1146/annurev-ento-120709144855.
3. Matsumoto Y, Mizunami M. Olfactory learning in
the cricket Gryllus bimaculatus. J Exp Biol 2000,
203:25812588.
4. Giurfa M. Behavioral and neural analysis of associative
learning in the honeybee: a taste from the magic well.
J Comp Physiol A 2007, 193:801824.
5. Menzel R. Memory dynamics in the honeybee. J Comp
Physiol A 1999, 185:323340.
6. Dupuy F, Sandoz JC, Giurfa M, Josens R. Individual
olfactory learning in Camponotus ants. Anim Behav
2006, 72:10811091.
7. Daly KC, Smith BH. Associative olfactory learning in the moth Manduca Sexta. J Exp Biol 2000,
203:20252038.

8. Vergoz V, Roussel E, Sandoz JC, Giurfa M. Aversive learning in honeybees revealed by the olfactory
conditioning of the sting extension reflex. PLoS One
2007, 2:e288.
9. Davis RL. Olfactory memory formation in Drosophila:
from molecular to systems neuroscience. Annu Rev
Neurosci 2005, 28:275302.
10. Fiala A. Olfaction and olfactory learning in Drosophila:
recent progress. Curr Opin Neurobiol 2007,
17:720726.
11. Keene AC, Waddell S. Drosophila olfactory memory:
single genes to complex neural circuits. Nat Rev Neurosci 2007, 8:341354.
12. Busto GU, Cervantes-Sandoval I, Davis RL. Olfactory
learning in Drosophila. Physiology (Bethesda) 2010,
25:338346.
13. Guven-Ozkan T, Davis RL. Functional neuroanatomy
of Drosophila olfactory memory formation. Learn Mem
2014, 21:519526.
14. Davis RL. Traces of drosophila memory. Neuron 2011,
70:819.

2015 John Wiley & Sons, Ltd.

wires.wiley.com/cogsci

Advanced Review

15. Menzel R. Searching for the memory trace in a

mini-brain, the honeybee. Learn Mem 2001, 8:5362.
16. Strausfeld NJ. Arthropod Brains: Evolution, Functional
Elegance, and Historical Significance. Cambridge, MA:
Belknap Press; 2012.
17. Ramn y Cajal S, Snchez D. Contribucin al
Conocimiento de los Centros Nerviosos de los Insectos.
Madrid: Imprenta de Hijos de Nicols Moya; 1915.
18. Pavlov IP, Anrep GV. Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral
Cortex. London: Oxford University Press; 1927.
19. Skinner BF. The Behavior of Organisms: An Experimental Analysis. New York: Appleton-Century-Crofts;
1938.
20. van Swinderen B, Greenspan RJ. Salience modulates
2030 Hz brain activity in Drosophila. Nat Neurosci
2003, 6:579586.
21. Spaethe J, Tautz J, Chittka L. Do honeybees detect
colour targets using serial or parallel visual search?
J Exp Biol 2006, 209:987993.
22. Dawson EH, Avargus-Weber A, Chittka L, Leadbeater
E. Learning by observation emerges from simple associations in an insect model. Curr Biol 2013, 23:727730.
23. Worden BD, Papaj DR. Flower choice copying in
bumblebees. Biol Lett 2005, 1:504507.
24. Leadbeater E, Chittka L. A new mode of information transfer in foraging bumblebees? Curr Biol 2005,
15:R447R448.
25. Leadbeater E, Chittka L. The dynamics of social learning in an insect model, the bumblebee (Bombus terrestris). Behav Ecol Sociobiol 2007, 61:17891796.
26. Battesti M, Moreno C, Joly D, Mery F. Spread of social
information and dynamics of social transmission within
Drosophila groups. Curr Biol 2012, 22:309313.
27. Coolen I, Dangles O, Casas J. Social learning in noncolonial insects? Curr Biol 2005, 15:19311935.
28. Sheehan MJ, Tibbetts EA. Specialized face learning is
associated with individual recognition in paper wasps.
Science 2011, 334:12721275.
29. Tibbetts EA. Visual signals of individual identity
in the wasp Polistes fuscatus. Proc Biol Sci 2002,
269:14231428.
30. Tibbetts EA, Dale J. A socially enforced signal of quality
in a paper wasp. Nature 2004, 432:218222.
31. Benard J, Stach S, Giurfa M. Categorization of visual
stimuli in the honeybee Apis mellifera. Anim Cogn
2006, 9:257270.
32. Giurfa M, Zhang S, Jenett A, Menzel R, Srinivasan MV.
The concepts of sameness and difference in an insect.
Nature 2001, 410:930933.
33. Avargus-Weber A, Dyer AG, Giurfa M. Conceptualization of above and below relationships by an insect. Proc
Biol Sci 2011, 278:898905.

34. Avargus-Weber A, Dyer AG, Combe M, Giurfa M.

Simultaneous mastering of two abstract concepts by the
miniature brain of bees. Proc Natl Acad Sci USA 2012,
109:74817486.
35. Perry CJ, Barron AB. Honey bees selectively avoid
difficult choices. Proc Natl Acad Sci USA 2013,
110:1915519159.
36. Bitterman ME, Menzel R, Fietz A, Schfer S. Classical
conditioning of proboscis extension in honeybees (Apis
mellifera). J Comp Psychol 1983, 97:107119.
37. Giurfa M, Sandoz JC. Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis
extension response in honeybees. Learn Mem 2012,
19:5466.
38. Takeda K. Classical conditioned response in the honey
bee. J Insect Physiol 1961, 6:168179.
39. Watanabe H, Mizunami M. Pavlovs cockroach: classical conditioning of salivation in an insect. PLoS One
2007, 2:e529.
40. Tully T, Quinn WG. Classical conditioning and retention in normal and mutant Drosophila melanogaster.
J Comp Physiol Psychol 1985, 156:263277.
41. von Frisch K. Der Farbensinn und Formensinn der
Biene. Zool Jahrb Abt Allg Zool Physiol Tiere 1914,
37:1238.
42. Gtz KG. Optomotorische Untersuchung des visuellen
Systems einiger Augenmutanten der Fruchtfliege
Drosophila. Kybernetik 1964, 2:7792.
43. Heisenberg M, Wolf R, Brembs B. Flexibility in a single
behavioral variable of Drosophila. Learn Mem 2001,
8:110.
44. Brembs B, Heisenberg M. The operant and the classical
in conditioned orientation of Drosophila melanogaster
at the flight simulator. Learn Mem 2000, 7:104115.
45. Wustmann G, Rein K, Wolf R, Heisenberg M. A
new paradigm for operant conditioning of Drosophila
melanogaster. J Comp Physiol A 1996, 179:429436.
46. Putz G, Heisenberg M. Memories in drosophila
heat-box learning. Learn Mem 2002, 9:349359.
47. Vinauger C, Lallement H, Lazzari CR. Learning and
memory in Rhodnius prolixus: habituation and aversive operant conditioning of the proboscis extension
response. J Exp Biol 2013, 216:892900.
48. Pearce JM. Animal Learning and Conditioning: an
Introduction. Hove: Psychology Press; 1997.
49. Giurfa M. Conditioning procedure and color discrimination in the honeybee Apis mellifera. Naturwissenschaften 2004, 91:228231.
50. Dyer AG, Chittka L. Fine colour discrimination
requires differential conditioning in bumblebees.
Naturwissenschaften 2004, 91:224227.
51. Avargus-Weber A, Giurfa M. Cognitive components of
color vision in honey bees: how conditioning variables
modulate color learning and discrimination. J Comp
Physiol A 2014, 200:449461.

2015 John Wiley & Sons, Ltd.

WIREs Cognitive Science

Learning and insect cognition

52. Tang S, Juusola M. Intrinsic activity in the fly brain gates

visual information during behavioral choices. PLoS
One 2010, 5:e14455.

68. Zentall TR, Galizio M, Critchfield TS. Categorization,

concept learning, and behavior analysis: an introduction. J Exp Anal Behav 2002, 78:237248.

53. von Frisch K. The Dance Language and Orientation of

Bees. Cambridge: Harvard University Press; 1967.

69. Zentall TR, Wasserman EA, Lazareva OF, Thompson

RKR, Rattermann MJ. Concept learning in animals.
Comp Cogn Behav Rev 2008, 3:1345.

54. Grter C, Farina WM. The honeybee waggle dance:

can we follow the steps? Trends Ecol Evol 2009,
24:242247.
55. Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel
R. The flight paths of honeybees recruited by the waggle
dance. Nature 2005, 435:205207.
56. Seeley TD. Honeybee Democracy. Princeton, NJ:
Princeton University Press; 2010.
57. Arenas A, Fernndez VM, Farina WM. Floral odor
learning within the hive affects honeybees foraging
decisions. Naturwissenschaften 2007, 94:218222.
58. Gil M, De Marco RJ. Olfactory learning by means
of trophallaxis in Apis mellifera. J Exp Biol 2005,
208:671680.
59. Leadbeater E, Chittka L. Social transmission of
nectar-robbing behaviour in bumble-bees. Proc Biol Sci
2008, 275:16691674.
60. Mery F, Varela SAM, Danchin E, Blanchet S, Parejo
D, Coolen I, Wagner RH. Public versus personal information for mate copying in an invertebrate. Curr Biol
2009, 19:730734.
61. Tabone CJ, de Belle S. Second-order conditioning in
Drosophila. Learn Mem 2011, 18:250253.
62. Grossmann KE. Belohnungsverzgerung beim Erlernen
einer Farbe an einer knstlichen Futterstelle durch
Honigbienen. Z Tierpsychol 1971, 29:2841.
63. Galizia CG, Menzel R. The role of glomeruli in the
neural representation of odours: results from optical
recording studies. J Insect Physiol 2001, 47:115129.

70. Murphy GL. The Big Book of Concepts. Cambridge,

MA: MIT Press; 2002.
71. Murphy GL. What are categories and concepts? In:
Mareschal D, Quinn PC, Lea SEG, eds. The Making of
Human Concepts. New York: Oxford University Press;
2010, 1128.
72. Zhang SW, Srinivasan MV, Zhu H, Wong J. Grouping
of visual objects by honeybees. J Exp Biol 2004,
207:32893298.
73. Zhang SW, Bock F, Si A, Tautz J, Srinivasan MV. Visual
working memory in decision making by honey bees.
Proc Natl Acad Sci USA 2005, 102:52505255.
74. Chittka L, Jensen K. Animal cognition: concepts from
apes to bees. Curr Biol 2011, 21:R116R119.
75. Avargus-Weber A, DAmaro D, Metzler M, Dyer
AG: Conceptualization of relative size by honeybees. Front Behav Neurosci 2014, 8:80. doi:10.3389/
fnbeh.2014.00080.
76. Terrace HS, Son LK. Comparative metacognition. Curr
Opin Neurobiol 2009, 19:6774.
77. Hampton RR. Multiple demonstrations of metacognition in nonhumans: converging evidence or multiple
mechanisms? Comp Cogn Behav Rev 2009, 4:1728.
78. Menzel R, Giurfa M. Cognitive architecture of a
mini-brain: the honeybee. Trends Cogn Sci 2001,
5:6271.

64. DEttorre P, Heinze J. Individual recognition in ant

queens. Curr Biol 2005, 15:21702174.

79. Dyer AG. The mysterious cognitive abilities of bees: why

models of visual processing need to consider experience
and individual differences in animal performance. J Exp
Biol 2012, 215:387395.

65. Stach S, Benard J, Giurfa M. Local-feature assembling

in visual pattern recognition and generalization in honeybees. Nature 2004, 429:758761.

80. Giurfa M. Cognitive neuroethology: dissecting

non-elemental learning in a honeybee brain. Curr
Opin Neurobiol 2003, 13:726735.

66. Avargus-Weber A, Portelli G, Benard J, Dyer A, Giurfa

M. Configural processing enables discrimination and
categorization of face-like stimuli in honeybees. J Exp
Biol 2010, 213:593601.

81. Zhang SW, Si A, Pahl M. Visually guided decision

making in foraging honeybees. Front Neurosci 2012,
6:88.

67. Robertson SI. Problem Solving. Hove: Psychology Press;

2001.

82. Srinivasan MV. Honey bees as a model for vision,

perception, and cognition. Annu Rev Entomol 2010,
55:267284.

FURTHER READING/RESOURCES
Giurfa M. Cognition with few neurons: higher-order learning in insects. Trends Neurosci 2013, 36:285294.
doi:10.1016/j.tins.2012.12.011.
North G, Grenspan RJ. Invertebrate Neurobiology. Cold Spring Harbor Monograph Series 49. New York: Cold Spring
Harbor Laboratory Press; 2007.

2015 John Wiley & Sons, Ltd.