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Norm-based face encoding by single neurons in the monkey inferotemporal cortex

Nature volume 442, pages 572–575 (2006)Cite this article

Abstract

The rich and immediate perception of a familiar face, including its identity, expression and even intent, is one of the most impressive shared faculties of human and non-human primate brains. Many visually responsive neurons in the inferotemporal cortex of macaque monkeys respond selectively to faces1,2,3,4, sometimes to only one or a few individuals5,6,7, while showing little sensitivity to scale and other details of the retinal image8,9. Here we show that face-responsive neurons in the macaque monkey anterior inferotemporal cortex are tuned to a fundamental dimension of face perception. Using a norm-based caricaturization framework previously developed for human psychophysics10,11,12, we varied the identity information present in photo-realistic human faces13, and found that neurons of the anterior inferotemporal cortex were most often tuned around the average, identity-ambiguous face. These observations are consistent with face-selective responses in this area being shaped by a figural comparison, reflecting structural differences between an incoming face and an internal reference or norm. As such, these findings link the tuning of neurons in the inferotemporal cortex to psychological models of face identity perception.

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Figure 1: Face space and behavioural data.
Figure 2: Responses of a single neuron (C99-117) to faces along axes of caricaturization.
Figure 3: Response magnitudes for different caricaturization levels of all four faces.
Figure 4: Population responses as a function of the caricaturization level.
Figure 5: Responses to radial and tangential morphs.

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Acknowledgements

We are grateful to G. Rhodes, N. Kriegeskorte and N. K. Logothetis for critical comments on the manuscript, and to A. Maier, M. Wilke and K.-M. Mueller for discussions. We especially thank C. Wallraven, B. Knappmeyer and H. H. Bülthoff for conducting experiments aimed at selecting the perceptually most dissimilar faces serving as the stimuli for C99. This work was executed at the Max Planck Institute for Biological Cybernetics, and was supported by a Max Planck Society grant to N. K. Logothetis, as well as grants from the Volkswagen Foundation, DFG and HFSP (to M.A.G.). Author Contributions D.A.L and I.V.B originated the experiment and performed the neurophysiological recordings. All authors performed data analysis and discussed the results. D.A.L. and M.A.G. wrote the paper.

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Author notes

  1. David A. Leopold

    Present address: Unit on Cognitive Neurophysiology and Imaging, Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, 49 Convent Drive, Bldg. 49, MSC 4400, Bethesda, Maryland, 20892, USA

  2. Igor V. Bondar

    Present address: Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Butlerova Street 5a, 117485, Moscow, Russia

Authors and Affiliations

  1. Max Planck Institut für biologische Kybernetik, Spemannstrasse 38, 72076, Tübingen, Germany

    David A. Leopold & Igor V. Bondar

  2. Laboratory for Action Representation and Learning, Department of Cognitive Neurology, Hertie Institute for Clinical Brain Research, University Clinic Tübingen, Schaffhausenstr. 113, D-72072, Tübingen, Germany

    Martin A. Giese

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Correspondence to David A. Leopold.

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Supplementary Notes

This file contains Supplementary Methods, Supplementary Figures 1–11 and legends, Supplementary Tables 1 and 2 and legends, and seven references. (PDF 1075 kb)

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Leopold, D., Bondar, I. & Giese, M. Norm-based face encoding by single neurons in the monkey inferotemporal cortex. Nature 442, 572–575 (2006). https://doi.org/10.1038/nature04951

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