(Translated by https://www.hiragana.jp/)
A face feature space in the macaque temporal lobe | Nature Neuroscience
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.

  • Article
  • Published:

A face feature space in the macaque temporal lobe

Nature Neuroscience volume 12, pages 1187–1196 (2009)Cite this article

Abstract

The ability of primates to effortlessly recognize faces has been attributed to the existence of specialized face areas. One such area, the macaque middle face patch, consists almost entirely of cells that are selective for faces, but the principles by which these cells analyze faces are unknown. We found that middle face patch neurons detect and differentiate faces using a strategy that is both part based and holistic. Cells detected distinct constellations of face parts. Furthermore, cells were tuned to the geometry of facial features. Tuning was most often ramp-shaped, with a one-to-one mapping of feature magnitude to firing rate. Tuning amplitude depended on the presence of a whole, upright face and features were interpreted according to their position in a whole, upright face. Thus, cells in the middle face patch encode axes of a face space specialized for whole, upright faces.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: Selectivity of the middle face patch for real and cartoon faces.
Figure 2: Selectivity for face parts.
Figure 3: Cartoon tuning.
Figure 4: Preference for extreme feature values.
Figure 5: Joint tuning to feature dimension pairs.
Figure 6: Integration of features and effects of face context.
Figure 7: Face inversion and feature tuning.

Similar content being viewed by others

References

  1. Hubel, D.H. & Wiesel, T.N. Receptive fields of single neurones in the cat's striate cortex. J. Physiol. (Lond.) 148, 574–591 (1959).

    Article  CAS  Google Scholar 

  2. Kanwisher, N., McDermott, J. & Chun, M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 17, 4302–4311 (1997).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Brunswik, E. & Reiter, L. Eindruckscharaktere schematisierter Gesichter. Zeitschrift Fuer Psychologie 142, 67–135 (1937).

    Google Scholar 

  6. Biederman, I. Recognition-by-components: a theory of human image understanding. Psychol. Rev. 94, 115–147 (1987).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Benson, P.J. & Perrett, D.I. Perception and recognition of photographic quality facial carricatures: implications for the recognition of natural images. Eur. J. Cogn. Psychol. 3, 105–135 (1991).

    Article  Google Scholar 

  9. Leopold, D.A., Bondar, I.V. & Giese, M.A. Norm-based face encoding by single neurons in monkey inferotemporal cortex. Nature 442, 572–575 (2006).

    Article  CAS  Google Scholar 

  10. Mel, B. & Fiser, J. Minimizing binding errors using learned conjunctive features. Neural Comput. 12, 247–278 (2000).

    Article  CAS  Google Scholar 

  11. Grunewald, A. & Skoumbourdis, E.K. The integration of multiple stimulus features by V1 neurons. J. Neurosci. 24, 9185–9194 (2004).

    Article  CAS  Google Scholar 

  12. Young, A.W., Hellawell, D. & Hay, D.C. Configural information in face perception. Perception 16, 747–759 (1987).

    Article  CAS  Google Scholar 

  13. Tanaka, J.W. & Farah, M.J. Parts and wholes in face recognition. Q. J. Exp. Psychol. A. 46, 225–245 (1993).

    Article  CAS  Google Scholar 

  14. Thompson, P. Margaret Thatcher: a new illusion. Perception 9, 483–484 (1980).

    Article  CAS  Google Scholar 

  15. Yin, R.K. Looking at upside-down faces. J. Exp. Psychol. 81, 141–145 (1969).

    Article  Google Scholar 

  16. Bartlett, J.C. & Searcy, J. Inversion and configuration of faces. Cogn. Psychol. 25, 281–316 (1993).

    Article  CAS  Google Scholar 

  17. Brincat, S.L. & Connor, C.E. Underlying principles of visual shape selectivity in posterior inferior temporal cortex. Nat. Neurosci. 7, 880–886 (2004).

    Article  CAS  Google Scholar 

  18. 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 

  19. McKone, E., Aitkin, A. & Edwards, M. Categorical and coordinate relations in faces, or Fechner's law and face space instead? J. Exp. Psychol. Hum. Percept. Perform. 31, 1181–1198 (2005).

    Article  Google Scholar 

  20. Fraser, I.H., Craig, G.L. & Parker, D.M. Reaction time measures of feature saliency in schematic faces. Perception 19, 661–673 (1990).

    Article  Google Scholar 

  21. Guigon, E. Computing with populations of monotonically tuned neurons. Neural Comput. 15, 2115–2127 (2003).

    Article  Google Scholar 

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

    Article  Google Scholar 

  23. De Baene, W., Premereur, E. & Vogels, R. Properties of shape tuning of macaque inferior temporal neurons examined using rapid serial visual presentation. J. Neurophysiol. 97, 2900–2916 (2007).

    Article  Google Scholar 

  24. Rhodes, G. Superportraits: Caricatures and Recognition (Psychology Press Publishers, East Sussex, UK, 1996).

    Google Scholar 

  25. Webster, M.A. & MacLin, O. Figural aftereffects in the perception of faces. Psychon. Bull. Rev. 6, 647–653 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Quiroga, R.Q., Reddy, L., Kreiman, G., Koch, C. & Fried, I. Invariant visual representation by single neurons in the human brain. Nature 435, 1102–1107 (2005).

    Article  CAS  Google Scholar 

  28. Zhang, K. & Sejnowski, T.J. Neuronal tuning: to sharpen or broaden? Neural Comput. 11, 75–84 (1999).

    Article  CAS  Google Scholar 

  29. Eurich, C.W. & Wilke, S.D. Multidimensional encoding strategy of spiking neurons. Neural Comput. 12, 1519–1529 (2000).

    Article  CAS  Google Scholar 

  30. Galton, F. Composite portraits, made by combining those of many different persons into a single, resultant figure. J. Anthropol. Inst. 8, 132–144 (1879).

    Google Scholar 

  31. Salinas, E. & Thier, P. Gain modulation: a major computational principle of the central nervous system. Neuron 27, 15–21 (2000).

    Article  CAS  Google Scholar 

  32. Liu, Y. & Jagadeesh, B. Neural selectivity in anterior inferotemporal cortex for morphed photographic images during behavioral classification or fixation. J. Neurophysiol. 100, 966–982 (2008).

    Article  Google Scholar 

  33. Andersen, R.A., Bracewell, R.M., Barash, S., Gnadt, J.W. & Fogassi, L. Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J. Neurosci. 10, 1176–1196 (1990).

    Article  CAS  Google Scholar 

  34. Zipser, D. & Andersen, R.A. A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331, 679–684 (1988).

    Article  CAS  Google Scholar 

  35. Treue, S. & Martínez Trujillo, J.C. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999).

    Article  CAS  Google Scholar 

  36. Koida, K. & Komatsu, H. Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex. Nat. Neurosci. 10, 108–116 (2007).

    Article  CAS  Google Scholar 

  37. Thorpe, S., Fize, D. & Marlot, C. Speed of processing in the human visual system. Nature 381, 520–522 (1996).

    Article  CAS  Google Scholar 

  38. Keysers, C., Xiao, D.-K., Földiák, P. & Perrett, D.I. The speed of sight. J. Cogn. Neurosci. 13, 90–101 (2001).

    Article  CAS  Google Scholar 

  39. Fabre-Thorpe, M., Richard, G. & Thorpe, S.J. Rapid categorization of natural images by rhesus monkeys. Neuroreport 9, 303–308 (1998).

    Article  CAS  Google Scholar 

  40. Cox, D., Meyers, E. & Sinha, P. Contextually evoked object-specific responses in human visual cortex. Science 304, 115–117 (2004).

    Article  CAS  Google Scholar 

  41. McAdams, C.J. & Maunsell, J.H.R. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431–441 (1999).

    Article  CAS  Google Scholar 

  42. Tanaka, K., Saito, H.-A., Fukada, Y. & Moriya, M. Coding visual images of objects in the inferotemporal cortex of the macaque monkey. J. Neurophysiol. 66, 170–189 (1991).

    Article  CAS  Google Scholar 

  43. Fujita, I., Tanaka, K., Ito, M. & Cheng, K. Columns for visual features of objects in monkey inferotemporal cortex. Nature 360, 343–346 (1992).

    Article  CAS  Google Scholar 

  44. Wang, G., Tanaka, K. & Tanifuji, M. Optical imaging of functional organization in the monkey inferotemporal cortex. Science 272, 1665–1668 (1996).

    Article  CAS  Google Scholar 

  45. Bruce, C., Desimone, R. & Gross, C.G. Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol. 46, 369–384 (1981).

    Article  CAS  Google Scholar 

  46. Baylis, G.C., Rolls, E.T. & Leonard, C.M. Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Res. 342, 91–102 (1985).

    Article  CAS  Google Scholar 

  47. Perrett, D.I. et al. Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc. R. Soc. Lond. B 223, 293–317 (1985).

    Article  CAS  Google Scholar 

  48. Zar, J.H. Biostatistical Analysis (Prentice Hall, Upper Saddle River, New Jersey, 1998).

    Google Scholar 

  49. Efron, B. Bootstrap methods: another look at the jackknife. Ann. Stat. 7, 1–26 (1979).

    Article  Google Scholar 

  50. Manly, B.F.J. Randomization, Bootstrap and Monte Carlo Methods in Biology (CRC Press, Boca Raton, Florida, 2007).

    Google Scholar 

Download references

Acknowledgements

We are grateful to the late D. Freeman and N. Nallasamy for stimulus programming; R. Tootell, W. Vanduffel and members of the Massachusetts General Hospital monkey fMRI group for assistance with scanning; A. Dale and A. van der Kouwe for allowing us to use their multi-echo sequence and undistortion algorithm; T. Chuprina and N. Schweers for animal care and Guerbet for providing Sinerem contrast agent. This work was sponsored by US National Institutes of Health grant EY16187 and German Science Foundation grant FR 1437/3-1. D.Y.T. was supported by a Sofja Kovalevskaja Award from the Alexander von Humboldt Foundation.

Author information

Author notes

  1. Winrich A Freiwald and Doris Y Tsao: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, USA

    Winrich A Freiwald, Doris Y Tsao & Margaret S Livingstone

  2. Centers for Advanced Imaging & Cognitive Sciences, Bremen University, Bremen, Germany

    Winrich A Freiwald & Doris Y Tsao

  3. Division of Biology, California Institute of Technology, Pasadena, California, USA

    Winrich A Freiwald & Doris Y Tsao

  4. The Rockefeller University, New York, New York, USA

    Winrich A Freiwald

  5. Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts, USA

    Doris Y Tsao

Authors
  1. Winrich A Freiwald
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doris Y Tsao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Margaret S Livingstone
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Winrich A Freiwald.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Freiwald, W., Tsao, D. & Livingstone, M. A face feature space in the macaque temporal lobe. Nat Neurosci 12, 1187–1196 (2009). https://doi.org/10.1038/nn.2363

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2363

This article is cited by

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