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New Research, Cognition and Behavior

Color tuning of face-selective neurons in macaque inferior temporal cortex

Marianne Duyck, Audrey L.Y. Chang, Tessa J. Gruen, Lawrence Y. Tello, Serena Eastman, Joshua Fuller-Deets and Bevil Conway
eNeuro 22 January 2021, ENEURO.0395-20.2020; DOI: https://doi.org/10.1523/ENEURO.0395-20.2020
Marianne Duyck
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Audrey L.Y. Chang
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Tessa J. Gruen
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Lawrence Y. Tello
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Serena Eastman
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Joshua Fuller-Deets
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Bevil Conway
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, MD 20982-4435
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Abstract

What role does color play in the neural representation of complex shapes? We approached the question by measuring color responses of face-selective neurons, using fMRI-guided microelectrode recording of the middle and anterior face patches of inferior temporal cortex (IT) in rhesus macaques. Face-selective cells responded weakly to pure color (equiluminant) photographs of faces. But many of the cells nonetheless showed a bias for warm colors when assessed using images that preserved the luminance contrast relationships of the original photographs. This bias was also found for non-face-selective neurons. Fourier analysis uncovered two components: the first harmonic, accounting for most of the tuning, was biased towards reddish colors, corresponding to the L>M pole of the L-M cardinal axis. The second harmonic showed a bias for modulation between blue and yellow colors axis, corresponding to the S-cone axis. To test what role face-selective cells play in behavior, we related the information content of the neural population with the distribution of face colors. The analyses show that face-selective cells are not optimally tuned to discriminate face colors, but are consistent with the idea that face-selective cells contribute selectively to processing the green-red contrast of faces. The research supports the hypothesis that color-specific information related to the discrimination of objects, including faces, is handled by neural circuits that are independent of shape-selective cortex, as captured by the multi-stage parallel processing framework of IT (Lafer-Sousa and Conway, Nature Neuroscience, 2013).

SignificanceDoes the brain encode face-specific color signals, such as those related to health and emotion, through color responses of face-selective neurons? This paper addresses this question by providing the first, to our knowledge, quantitative measurements of the color-tuning of face-selective cells. Face-selective cells are not very responsive to pure color (equiluminant) pictures of faces. But both face-selective and non-face-selective cells are biased for warm colors. Information analysis shows that face-selective cells are not optimally tuned to discriminate face colors but suggests that the cells may contribute to discriminating the reddish component of faces. Alternatively, face-cell color tuning may reflect a broader adaptation of IT for the detection of objects, which are, in general, characterized by warmer coloring compared to backgrounds.

  • color vision
  • face perception
  • inferior temporal cortex
  • inferotemporal cortex
  • neurophysiology
  • social signaling

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by the Intramural research program of the National Eye Institute and the National Institute of Mental Health at the National Institutes of Health.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Color tuning of face-selective neurons in macaque inferior temporal cortex
Marianne Duyck, Audrey L.Y. Chang, Tessa J. Gruen, Lawrence Y. Tello, Serena Eastman, Joshua Fuller-Deets, Bevil Conway
eNeuro 22 January 2021, ENEURO.0395-20.2020; DOI: 10.1523/ENEURO.0395-20.2020

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Color tuning of face-selective neurons in macaque inferior temporal cortex
Marianne Duyck, Audrey L.Y. Chang, Tessa J. Gruen, Lawrence Y. Tello, Serena Eastman, Joshua Fuller-Deets, Bevil Conway
eNeuro 22 January 2021, ENEURO.0395-20.2020; DOI: 10.1523/ENEURO.0395-20.2020
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Keywords

  • color vision
  • face perception
  • inferior temporal cortex
  • inferotemporal cortex
  • neurophysiology
  • social signaling

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