Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

References

  1. Perrett, D. I., Rolls, E. T. & Caan, W. Visual neurones responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329–342 (1982)

    Article  CAS  Google Scholar 

  2. Gross, C. G. How inferior temporal cortex became a visual area. Cereb. Cortex 4, 455–469 (1994)

    Article  CAS  Google Scholar 

  3. Tsao, D. Y., Freiwald, W. A., Knutsen, T. A., Mandeville, J. B. & Tootell, R. B. Faces and objects in macaque cerebral cortex. Nature Neurosci. 6, 989–995 (2003)

    Article  CAS  Google Scholar 

  4. Logothetis, N. K. & Sheinberg, D. L. Visual object recognition. Annu. Rev. Neurosci. 19, 577–621 (1996)

    Article  CAS  Google Scholar 

  5. Hasselmo, M. E., Rolls, E. T. & Baylis, G. C. The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav. Brain Res. 32, 203–218 (1989)

    Article  CAS  Google Scholar 

  6. Sugase, Y., Yamane, S., Ueno, S. & Kawano, K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 869–873 (1999)

    Article  ADS  CAS  Google Scholar 

  7. Perrett, D. I. et al. Neurones responsive to faces in the temporal cortex: studies of functional organization, sensitivity to identity and relation to perception. Hum. Neurobiol. 3, 197–208 (1984)

    CAS  PubMed  Google Scholar 

  8. Rolls, E. T. & Baylis, G. C. Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey. Exp. Brain Res. 65, 38–48 (1986)

    Article  CAS  Google Scholar 

  9. Tovee, M. J., Rolls, E. T. & Azzopardi, P. Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. J. Neurophysiol. 72, 1049–1060 (1994)

    Article  CAS  Google Scholar 

  10. Rhodes, G., Brennan, S. & Carey, S. Identification and ratings of caricatures: implications for mental representations of faces. Cogn. Psychol. 19, 473–497 (1987)

    Article  CAS  Google Scholar 

  11. Valentine, T. & Bruce, V. The effects of distinctiveness in recognising and classifying faces. Perception 15, 525–535 (1986)

    Article  CAS  Google Scholar 

  12. Leopold, D. A., O'Toole, A. J., Vetter, T. & Blanz, V. Prototype-referenced shape encoding revealed by high-level aftereffects. Nature Neurosci. 4, 89–94 (2001)

    Article  CAS  Google Scholar 

  13. Blanz, V. & Vetter, T. in Proc. SIGGRAPH'99 187–194 (ACM, Computer Society Press, 1999)

    Book  Google Scholar 

  14. Lee, K., Byatt, G. & Rhodes, G. Caricature effects, distinctiveness, and identification: testing the face-space framework. Psychol. Sci. 11, 379–385 (2000)

    Article  CAS  Google Scholar 

  15. Lewis, M. B. & Johnston, R. A. Understanding caricatures of faces. Q. J. Exp. Psychol. A 51, 321–346 (1998)

    Article  CAS  Google Scholar 

  16. Mauro, R. & Kubovy, M. Caricature and face recognition. Mem. Cogn. 20, 433–440 (1992)

    Article  CAS  Google Scholar 

  17. Valentine, T. A unified account of the effects of distinctiveness, inversion, and race in face recognition. Q. J. Exp. Psychol. A 43, 161–204 (1991)

    Article  CAS  Google Scholar 

  18. Rhodes, G., et al. in Fitting the Mind to the World: Adaptation and Aftereffects in High-Level Vision (eds Clifford, C. W. & Rhodes, G.) 213–240 (Oxford Univ. Press, Oxford, UK, 2005)

    Google Scholar 

  19. Leopold, D. A., Rhodes, G., Mueller, K. M. & Jeffery, L. Dynamics of the face identity aftereffect. Proc. R. Soc. Lond. B 272, 897–904 (2005)

    Article  Google Scholar 

  20. Leopold, D. A. & Bondar, I. in Fitting the Mind to the World: Adaptation and Aftereffects in High-Level Vision (eds Clifford, C. W. G. & Rhodes, G.) 189–212 (Oxford Univ. Press, Oxford, UK, 2005)

    Google Scholar 

  21. Tsao, D. Y., Freiwald, W. A., Tootell, R. B. & Livingstone, M. S. A cortical region consisting entirely of face-selective cells. Science 311, 670–674 (2006)

    Article  ADS  CAS  Google Scholar 

  22. Sigala, N. & Logothetis, N. K. Visual categorization shapes feature selectivity in the primate temporal cortex. Nature 415, 318–320 (2002)

    Article  ADS  CAS  Google Scholar 

  23. Baker, C. I., Behrmann, M. & Olson, C. R. Impact of learning on representation of parts and wholes in monkey inferotemporal cortex. Nature Neurosci. 5, 1210–1216 (2002)

    Article  CAS  Google Scholar 

  24. Kobatake, E., Wang, G. & Tanaka, K. Effects of shape-discrimination training on the selectivity of inferotemporal cells in adult monkeys. J. Neurophysiol. 80, 324–330 (1998)

    Article  CAS  Google Scholar 

  25. Persson, J., Habib, R. & Nyberg, L. Decreased activity in inferotemporal cortex during explicit memory: dissociating priming, novelty detection, and recognition. Neuroreport 13, 2181–2185 (2002)

    Article  Google Scholar 

  26. Kayaert, G., Biederman, I., Op de Beeck, H. P. & Vogels, R. Tuning for shape dimensions in macaque inferior temporal cortex. Eur. J. Neurosci. 22, 212–224 (2005)

    Article  Google Scholar 

Download references

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.

Author information

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

Authors
  1. David A. Leopold
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Igor V. Bondar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin A. Giese
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David A. Leopold.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

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)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04951

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing