variability in ring rates in areas such as MT and MST

(even when the exact same stimulus is presented) is the

basis for the animals decision and accounts for the
observed correlation between neuronal and psychophysical
behavior. This interpretation is strengthened by the nding
that microstimulating directional cells in area MTcreates a
bias in the monkeys perceptual report towards the
stimulated neurons preferred direction [17]. However, the
inuence of feature-based attention could provide an
alternative interpretation of the link between neuronal
andbehavioral performance. Onthis view, the animals shift
of attention towards one of the two possible directions (or
depth planes in the cylinder experiments) would enhance
the response of neurons preferring this direction (or depth).
In summary, there is converging evidence that as one
ascends through the hierarchy of areas in the visual cortex
there is a transition from a neural representation
dominated by the sensory input to a representation
emphasizing the inputs perceptual interpretation and
the animals behavioral state. This gradient is apparent
using several experimental paradigms but it remains an
open issue whether independent mechanisms (for the
resolution of depth ambiguities, of directional ambiguities
and for decisions between opposite choices in high-noise
conditions) contribute to it, or if feature-based attention is
the major and unifying cause of the modulating
mechanism.
References
1 Kaas, J.H. (1989) Why does the brain have so many visual areas?
J. Cogn. Neurosci. 1, 121135
2 Williams, Z.M. et al. (2003) Parietal activity and the perceived
direction of ambiguous apparent motion. Nat. Neurosci. 6, 616623
3 Van Essen, D.A. and Maunsell, J.H.R. (1983) Hierarchical organization
and functional streams in the visual cortex. Trends Neurosci. 6,
370375
4 Felleman, D.J. and Van Essen, D.C. (1991) Distributed hierarchical
processing in the primate cerebral cortex. Cereb. Cortex 1, 147
5 Ungerleider, L.G. and Mishkin, M. (1982) Two cortical visual systems.
In Analysis of Visual Behavior (Ingle, D. et al., eds), pp. 549586, MIT
Press
6 DeYoe, E.A. and Van Essen, D.C. (1988) Concurrent processing
streams in monkey visual cortex. Trends Neurosci. 11, 219226
7 Parker, A.J. and Newsome, W.T. (1998) Sense and the single neuron:
Probing the physiology of perception. Annu. Rev. Neurosci. 21,
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8 Bradley, D.C. et al. (1998) Encoding of three-dimensional structure-
from-motion by primate area MT neurons. Nature 392, 714717
9 Dodd, J.V. et al. (2001) Perceptually bistable three-dimensional gures
evoke high choice probabilities in cortical area MT. J. Neurosci. 21,
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perception of multi-stable gures. Philos. Trans. R. Soc. Lond. B Biol.
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11 Treue, S. and Martinez Trujillo, J.C. (1999) Feature-based attention
inuences motion processing gain in macaque visual cortex. Nature
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12 McAdams, C.J. and Maunsell, J.H.R. (2000) Attention to both space
and feature modulates neuronal responses in macaque area V4.
J. Neurophysiol. 83, 17511755
13 Treue, S. and Maunsell, J.H.R. (1999) Effects of attention on the
processing of motion in macaque visual cortical areas MT and MST.
J. Neurosci. 19, 76037616
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behavioral performance and neuronal responses in middle temporal
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decision. Nature 341, 5254
16 Celebrini, S. and Newsome, W.T. (1994) Neuronal and psychophysical
sensitivity to motion signals in extrastriate area MSTof the macaque
monkey. J. Neurosci. 14, 41094124
17 Salzman, C.D. et al. (1990) Cortical microstimulation inuences
perceptual judgements of motion direction. Nature 346, 174177
1364-6613/$ - see front matter q 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.tics.2003.09.003
Wholes, holes, and basic features in vision
James R. Pomerantz
Department of Psychology, Rice University, Houston, Texas 77005, USA
A key issue for theories of perception is specifying the
primitives used by the visual system to isolate and
identify the objects in an image. Although local features
are typically suggested, there is good reason to look
for global, congural features as primitives too. Chen
et al.s specic proposal of topological features is both
explicit and capable of capturing important global infor-
mation. It may seem surprising that topology can be
detected by honeybees, but Chens results are in keep-
ing with other ndings from humans that global proper-
ties are sometimes perceived better than local ones and
thus might be basic.
The visual system informs organisms about their sur-
roundings, but how does it sort out the vast quantity of
information contained in an image? When facing a new
scene, where does the visual system start? Most theories
of vision begin with local features, such as oriented line
segments, and build up from there, using attention to
integrate features [1,2]. We have known, at least since the
Gestalt psychologists however [3], that global properties
often dominate perception. A recent paper by Lin Chen and
his colleagues [4] suggests an intriguing method by which
global properties might be detected early in the sequence.
The centrality of grouping
It seems sensible that the visual system must segment
a full scene into grouped regions before it attempts to Corresponding author: James R. Pomerantz (pomeran@rice.edu).
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recognize the objects within the scene, lest it engage in a
futile effort to integrate features belonging to separate
objects (e.g. combining the head of a horse with the arm of
its rider, or the eyes of one person with the mouth of
another). The nature of the grouping process that could
achieve such parsing remains elusive, however [5]. Many
Gestalt proposals for grouping factors and possible mech-
anisms are suggestive and promising, but often the Gestalt
laws of perceptual organization are expressed casually or
subjectively rather than being made explicit. Chen et al.s
suggestion that topological invariants are crucial gives us
a novel idea that is both explicit and capable of capturing
some global properties of images that can help solve the
grouping problem [6].
Primitives and derived properties
The search for primitives in vision features that are
processed rst has been dominated in the psycho-
physical realm by studies on visual search. Work by
Treisman [2], Wolfe [7], and others has revealed over a
dozen stimulus properties that will allow for rapid and
accurate detection (so-called pop-out) of targets irrespec-
tive of the number of background items in which they are
embedded. For example, a red disk will pop out immedi-
ately froma eld of green disks without sequential search-
ing, irrespective of the number of green disks. In their
paper, Chen et al. have suggested that topological proper-
ties are primitives for the honeybee visual system [4].
The notion that topological proprieties could be primi-
tives seems counterintuitive both because these properties
are generally regarded as complex and difcult to derive,
and because honeybees have limited nervous systems with
which to do the derivation. Nonetheless, we should bear in
mind two other observations. First, complexity is relative
to the organism. In the example with red and green disks,
we must remember that color is a complex property that is
difcult to derive. Color itself is not in the stimulus, of
course, but in the head. The stimulus does contain wave-
lengths, of course, but wavelengths per se do not pop out. In
fact, two stimuli with entirely different wavelength com-
ponents (spectra) can be metamers that is, can be indis-
tinguishable to the human eye. Chens data similarly
suggest that a hollow diamond and a ring two shapes
that are topologically equivalent might be metamers
for honeybees.
Second, we should be mindful that because a compu-
tation is difcult doesnt mean that it is beyond the cap-
ability of biological systems. Fourier analysis, for example,
is complex, but the human ear performs an approximation
using basic mechanical components as smart mechan-
isms, and computational shortcuts can also be found
(such as the fast Fourier transform). For these reasons, we
should take Chens nding on its own merits, without
prejudging it based on its seeming plausibility.
If properties such as topological invariants number of
holes, inside versus outside, and connectivity are com-
plex and can only be derived after extensive analysis, why
would such properties serve as primitives, as seems to be
the case for honeybees? The answer could lie in the adap-
tive value of derived or relational properties, or phrased
another way, in the lack of value of simple properties
including such absolutes as orientation, size and intensity.
These properties are often accidents of viewing conditions
(because, for example, the length of a line projected on the
retina varies with viewing angle) and so do not inform the
perceiver of important, invariant properties of the stimu-
lus [8,9]. For this reason, organisms might have evolved to
ignore these simple but less useful properties by routing
them through a sealed channel [10], where they are
unavailable for perception or for action but instead are fed
into systems that derive more complex properties from
them. Organisms might therefore rely on these emergent,
higher-order relational properties (beginning with simple
ratios and proportions and progressing towards more
complex ones involving topology), which remain invariant
under transformations. In this sense, we may say with
Gibson that they are perceived directly [11].
Congural superiority effects
An example of such a phenomenon in the shape domain
comes from the congural superiority effects that have
been studied in my laboratory and by others [12,13]. These
effects reveal an improvement in target detection by the
addition of context elements that create congurations,
even when those context elements alone provide no dis-
criminative information [14]. One example is shown in
Figure 1a. The task in the left panel is to locate a
negatively sloped diagonal target among three diagonals
with positive slopes. The center panel shows the context
(four identical L-shaped congurations), and the right
panel shows the superposition of the rst two panels
(target plus context). Although it might be thought that
Figure 1. (a) A congural superiority effect where differences in the slopes of
diagonal lines (left) are made more apparent by the addition of identical L-shaped
contexts (centre) that lead to the emergence of arrows and triangles (right).
(Adapted from [14].) (b,c) Possibly similar effects where topological differences
emerge that are highly salient: number of holes, and inside versus outside.
TRENDS in Cognitive Sciences
(a)
(b)
(c)
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adding identical Ls to the four diagonals would make the
target harder to spot (by masking or by diluting the
differences), in fact it makes the target far easier to spot:
the triangle in the right panel is perceptually more
different from the arrows than the negative diagonal in
the left panel is different from the positives, even though
the slope of that diagonal is all that distinguishes an arrow
from a triangle. Thus, sloped lines seem unlikely primi-
tives for recognizing such shapes. Instead, emergent topo-
logical properties that appear when the context is added
(properties such as the presence or absence of a hole) might
be the effective primitives.
Linking this work with Chens, it might be possible to
demonstrate other cases where topological factors domin-
ate early perception. Figure 1b shows a potential superi-
ority effect when identical disks are added both to small
rings and a large ring in a way that creates a topological
difference. Figure 1c shows another topological property
emerging from an added context, namely the inside/
outside relationship. Although these stimuli have not
been tested in a psychophysical experiment with humans,
it seems likely they will yield strong superiority effects.
That would provide further evidence supporting Chen
et al.s claim for topological features as primitives.
Isolating primitive factors
Converging operations such as these experiments would
provide are important, for the following reason. It is the
nature of visual forms that when a single aspect of a
shape is changed, many other aspects change as well. For
example, if one reduces the area of a stimulus, this will also
affect its perimeter. That creates problems for researchers
trying to show that particular features of shape determine
perception, for often there are other potential confounding
factors at work. The key to nding the effective primitives
in shape perception, I believe, is to broaden the base of
stimuli studied, and this perhaps stands as the key chal-
lenge for future research, be it with humans or honeybees,
horses or humpback whales.
References
1 Marr, D. (1982) Vision, Freeman Press
2 Treisman, A. and Gelade, G. (1980) A feature-integration theory of
attention. Cogn. Psychol. 12, 97136
3 Koffka, K. (1935/1963) Principles of Gestalt Psychology, Harcourt
Brace
4 Chen, L. et al. (2003) Global perception in small brains: topological
pattern recognition in honeybees. Proc. Natl. Acad. Sci. U. S. A. 100,
68846889
5 Palmer, S.E. (1999) Vision Science: Photons to Phenomenology, MIT
Press
6 Chen, L. (1982) Topological structure in visual perception. Science 218,
699700
7 Wolfe, J.M. (2003) Moving towards solutions to some enduring
controversies in visual search. Trends Cogn. Sci. 7, 7076
8 Biederman, I. (1987) Recognition by components: a theory of human
image understanding. Psychol. Rev. 94, 115147
9 Rock, I. (1983) The Logic of Perception, MIT Press
10 Pomerantz, J.R. (1978) Are complex visual features derived from
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E.L.J. and Buffart, H.F.J.M., eds), John Wiley
11 Gibson, J.J. (1966) The Senses Considered as Perceptual Systems,
Houghton Mifin
12 Enns, J.T. (1990) Three dimensional features that pop out in visual
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1364-6613/$ - see front matter q 2003 Published by Elsevier Ltd.
doi:10.1016/j.tics.2003.09.007
Statistical decision theory and evolution
Laurence T. Maloney
Department of Psychology, Center for Neural Science, New York University, 6 Washington Place, New York, NY 10003, USA
Two recent articles by Geisler and Diehl use Bayesian
statistical decision theory to model the co-evolution of
predator and prey in a simple, game-like environment.
The prey is characterized by its coloration. The predator
is characterized by the chromatic sensitivity of its visual
system and its willingness to attack. The authors
demonstrate how the coloration of prey and the percep-
tual system of the predator co-evolve, converging to a
Nash equilibrium for both species.
The visual systems of organisms are highly specialized [1]
and it is tempting to conclude that each specialization
must confer an advantage on the organism possessing it,
an advantage that ultimately translates into reproductive
success. The balance between predator and prey, for
example, can hinge on the preys ability to hide from the
predator or the predators ability to ferret out the prey.
Exactly how predator and prey co-evolve over time or how
this co-evolution shapes the characteristics of each is the
subject of two recent articles by Geisler and Diehl [2,3].
In these articles, Geisler and Diehl develop a model of
predatorprey interaction in a tiny environment where
prey differ only in the match between their coloration and
the typical background colors (camouage) and predators
differ in the chromatic sensitivities of their visual systems.
They investigate how natural selection would shape both
the chromatic sensitivity of the visual system of the
predator and the coloration of the prey.
Box 1 describes an organism that has already broken
out of the simply framework of Geisler and Diehls world. It Corresponding author: Laurence T. Maloney (Laurence.Maloney@nyu.edu).
Update TRENDS in Cognitive Sciences Vol.7 No.11 November 2003
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