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Correspondence

What can bees really tell us about the face processing system in humans?
Cognitive abilities present in humans, such as faceprocessing, are likely to have evolved under various
ecological pressures. A comparable and specialized faceprocessing system observed in sheep and non-human primatessuggests a possible common origin in evolution (Pascalis etal., 1999; Kendrick et al., 2001; Parr, 2003). However, it isimportant to determine when this system emerged during
evolution if we are to fully understand it. Studies conductedwith honeybees (Apis mellifera) and wasps (Polistes fuscatus)
could potentially contribute to our understanding of thisability.
Dyer et al. have demonstrated that bees are able to learn
and recognise the picture of a human face when paired witha novel face (Dyer et al., 2005), which is consistent with ourexisting knowledge of the bees’ visual ability. However, webelieve that Dyer’s extrapolations about how recognition isachieved and whether or not it is facilitated by specialised
brain regions are misleading.
Face recognition is carried out by an automated and specificprocess in humans, which is known as configural processing(perceiving metrical relations between face features).
Contrary to Dyer’s argument and to earlier research findings(Diamond and Carey, 1977), it is now debatable whether suchprocessing develops late in childhood (Schwarzer et al.,2005). Furthermore, studies that have created ‘visual experts’
who develop configural processing for non-face objects
require many more hours of intensive training than reported
by Dyer et al. In their study, there is no clear evidence ofconfigural processing and it is likely that the bees’ recognition
relied on specific features.
In human adults, functional neuroimaging studies haveidentified a network of areas within the ventral temporal
cortex that are highly responsive to faces (Haxby et al., 2000),with maximum selectivity in the right middle fusiform gyrus:
the so-called ‘fusiform face area’ (FFA) (Kanwisher et al.,1997). A comparable functional specialization supports faceprocessing in the primate brain (Tsao et al., 2006). Critically,
however, normal face identification relies on the integrity ofthis complex network, as prosopagnosic patients with lesions
sparing the FFA show impaired use of optimal informationfor face identification (Caldara et al., 2005; Schiltz et al.,2006).
With data collected from just five bees, it is too speculative
to conclude that specialised brain regions are not necessary forface processing in humans. Humans and bees have not shared
a common ancestor for roughly 600 million years and have
evolved very differently since this separation. We can therefore
expect them to process faces differently. Clearly, more studies

are required to determine how the honeybee succeeds in simple
face matching tasks before attempting to establish potentialsimilarities between its visual recognition abilities and those ofdifferent species. It is first necessary to establish whether bees
are able to recognise or categorise conspecifics in a similar way
to the wasp (Tibbetts, 2002; Tibbetts and Dale, 2004). Given
that humans appear capable of only processing faces confined
to human and non-human primate categories, it would besomewhat paradoxical if the bee demonstrated recognition withhuman faces but not with conspecifics. Finally, artificial
computing systems without a neural substrate also demonstrate
an optimal ability to recognize individual faces. Does such
evidence question the neural specificity of face processing inhumans?
doi:10.1242/jeb.02411

References
Caldara, R., Schyns. P., Mayer, E., Smith, M., Gosselin, F. and Rossion,
B. (2005). Does prosopagnosia take the eyes out of face representations?
Evidence for a defect in representing diagnostic facial information following
brain damage. J. Cog. Neurol. 17, 1652-1666.
Diamond, R. and Carey, S. (1977). Developmental changes in therepresentation of faces. J. Exp. Child Psychol. 23, 1-22.
Dyer, A. G., Neumeyer, C. and Chittka, L. (2005). Honeybee (Apismellifera) vision can discriminate between and recognise images of humanfaces. J. Exp. Biol. 208, 4709-4714.
Haxby, J. V., Hoffman, E. A. and Gobbini, M. I. (2000). The
distributed human neural system for face perception. Trends Cogn. Sci. 4,223-233.
Kanwisher, N., McDermott, J. and Chun, M. M. (1997). The fusiform facearea: a module in human extrastriate cortex specialized for face perception.
J. Neurosci. 17, 4302-4311.
Kendrick, K. N., da Costa, A. P., Leigh, A. E., Hinton, M. R. and Pierce,J. W. (2001). Sheep don’t forget a face. Nature 441, 165-166.
Parr, L. (2003). The discrimination of faces and their emotional contents bychimpanzees (Pan troglodytes). Ann. New. York. Acad. Sci. 1000, 56-78.
Pascalis, O., Petit, O., Kim, J. H. and Campbell, R. (1999). Picture
perception in primate: the case of face perception. Curr. Psychol. Cogn. 18,889-922.
Schiltz, C., Sorger, B., Caldara, R., Ahmed, F., Mayer, E., Goebel, R. andRossion, B. (2006). Impaired face discrimination in acquired prosopagnosia
is associated with abnormal response to individual faces in the right middle
fusiform gyrus. Cerebr. Cortex 16, 574-586.
Schwarzer, G., Huber, S. and Dümmler, T. (2005). Gaze behavior inanalytical and holistic face processing. Mem. Cog. 33, 344-354.
Tibbetts, E. A. (2002). Visual signals of individual identity in the wasp
Polistes fuscatus. Proc. R. Soc. Lond. B 269, 1423-1428.
Tibbetts, E. A. and Dale, J. (2004). A socially enforced signal of quality ina paper wasp. Nature 432, 218-222.
Tsao, D. Y., Winrich A., Freiwald, W. A., Tootell, R. B. H. andLivingstone, M. S. (2006). A cortical region consisting entirely of faceselective cells. Science 311, 670-674.

Olivier Pascalis1,*, David J. Kelly1 and Roberto Caldara2
1

Department of Psychology, The University of Sheffield, UK
2
Department of Psychology, University of Glasgow, UK*e-mail: o.pascalis@sheffield.ac.uk

THE JOURNAL OF EXPERIMENTAL BIOLOGYCorrespondence

3267

Response to ‘What can bees really tell us about the face processing system inhumans?’
Whilst humans have a large brain with regionalspecialization for solving complex tasks (Kandel et al., 2000),in certain cases the miniature brain of invertebrates performs
analogous tasks. For example, bees are capable of using topdown visual processing (Zhang and Srinivasan, 1994), canbalance conflicting speed accuracy demands in task allocation(Chittka et al., 2003), learn principles of symbolic matching(Giurfa et al., 2001), solve complex maze-type problems
and demonstrate context-dependent learning (Zhang andSrinivasan, 2004) and can use a symbolic coding system tocommunicate with conspecifics (von Frisch, 1967).
Studies of the capabilities of bees question the extent
to which large specialized brains are required to solve
sophisticated cognitive tasks (Zhang and Srinivasan, 2004).
What we can learn from the miniature brain is the extent towhich higher functions can be achieved without the complexity(and associated cost) of a large mammalian brain. For bees, it
is reasonably straightforward to control the ontogenetic history
of individuals, and if the bee’s brain can reveal novel solutions
for face processing this will potentially lead to algorithms for
artificial intelligence.
Our recent study (Dyer et al., 2005) does not exclude thepossibility that humans have regional specialization thatallows for fast processing of a relatively large number offaces (p. 4713). However, the finding that bees can recognize
stimuli representing human faces does question the extent
to which regional specialization is actually necessary for abrain to perform particular tasks; especially for reasonably
straightforward face recognition tasks (although even inhumans very few subjects score perfectly on Warrington facetests) (Warrington, 1996). It is clear from our study that somelevel of face recognition is possible from a miniature brain withabsolutely no evolutionary history for this task.
It is unlikely that bees will be able to recognize conspecifics
using facial cues, not because of a lack of cognitive ability but
because individual bees probably have insufficient facial
markings to enable a visual identification. An important factor
in the impressive conspecific face recognition capabilities of
paper wasps is that different individuals have specific facemarks (Tibbetts, 2002), which bees do not have. Even humans
are typically poor at recognizing face stimuli when the stimuli
class appears too similar; for example, recognizing individuals
from a different race category (Valentine and Endo, 1992).
Thus, it would not really be surprising if bees cannot recognize
conspecifics, even though it is clear that highly trained
individual bees are capable of recognizing human faces.
The study by Schwarzer et al. (Schwarzer et al., 2005) does
show some evidence that children use configural processing
less than adults (p. 352) and so does not fully discount the ideathat the visual system develops configural strategies withexperience. In agreement with previous work that demonstrates
that humans use feature extraction and configural processing
for face recognition (Collishaw and Hole, 2000), the study by
Schwarzer et al. presents evidence that humans use both feature
extraction and/or configural strategies (Schwarzer et al., 2005).
The interesting point from recent insect vision studies is thatbees also appear to use feature extraction and configuralprocessing depending upon level of experience with stimuli(Giurfa et al., 2003), and thus bees serve as a good model tounderstand how processes might operate in a miniature brain.
As visual strategies used by bees can potentially be whollytransferred to artificial intelligence applications (Srinivasan etal., 1997), this is an exciting model from which we might learna great deal.
doi:10.1242/jeb.02412

References
Chittka, L., Dyer A. G., Bock, F. and Dornhaus, A. (2003). Bees trade off
foraging speed for accuracy. Nature 424, 388.
Collishaw, S. M. and Hole, G. J. (2000). Featural and configuralprocesses in the recognition of faces of different familiarity. Perception
29, 893-909.
Dyer, A. G., Neumeyer, C. and Chittka, L. (2005). Honeybee (Apismellifera) vision can discriminate between and recognize images of humanfaces. J. Exp. Biol. 208, 4709-4714.
Giurfa, M., Zhang, S., Jenett, A., Menzel, R. and Srinivasan, M. V. (2001).
The concepts of ‘sameness’ and ‘difference’ in an insect. Nature 410, 930933.
Giurfa, M., Schubert, M., Reisenman, C., Gerber, B. and Lachnit, H.
(2003). The effect of cumulative experience on the use of elemental andconfigural visual discrimination strategies in honeybees. Behav. Brain. Res.
145, 161-169.
Kandel, E. R., Schwartz, J. H. and Jessell, T. M. (2000). Principles of NeuralScience. 4th edition. New York: McGraw Hill.
Schwarzer, G., Huber, S. and Dummler, T. (2005). Gaze behavior inanalytical and holistic face processing. Mem. Cog. 33, 344-354.
Srinivasan, M. V., Chahl, J. S., Nagle, M. G. and Zhang, S. W. (1997).
Embodying natural vision into machines. In From Living Eyes to Seeing
Machines (ed. M. V. Srinivasan and S. Venkatesh), pp. 249-265. Oxford:
Oxford University Press.
Tibbetts, E. A. (2002). Visual signals of individual identity in the wasp
Polistes fuscatus. Proc. R. Soc. Lond. B 269, 1423-1428.
Valentine, T. and Endo, M. (1992). Toward an exemplar model of faceprocessing: the effects of race and distinctiveness. Q. J. Exp. Psychol. 44A,161-204.
von Frisch, K. (1967). The Dance Language and Orientation of Bees. London,
UK: Harvard University Press.
Warrington, E. K. (1996). The Camden Memory Tests Manual. Windsor, UK:
Psychology Press.
Zhang, S. W. and Srinivasan, M. V. (1994). Prior experience enhances
pattern discrimination in insect vision. Nature 368, 330-332.
Zhang, S. W. and Srinivasan, M. (2004). Exploration of cognitive capacity
in honeybees: higher functions emerge from a small brain. In Complex
Worlds from Simpler Nervous Systems (ed. F. R. Prete), pp. 41-74.
Cambridge: MIT Press.

Adrian G. Dyer
Department of Physiology, Monash University, Clayton 3800,
Australiae-mail: a.dyer@latrobe.edu.au

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