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Microstimulation of inferotemporal cortex influences face categorization

A Corrigendum to this article was published on 05 October 2006

Abstract

The inferior temporal cortex (IT) of primates is thought to be the final visual area in the ventral stream of cortical areas responsible for object recognition1,2. Consistent with this hypothesis, single IT neurons respond selectively to highly complex visual stimuli such as faces3,4,5,6. However, a direct causal link between the activity of face-selective neurons and face perception has not been demonstrated. In the present study of macaque monkeys, we artificially activated small clusters of IT neurons by means of electrical microstimulation while the monkeys performed a categorization task, judging whether noisy visual images belonged to ‘face’ or ‘non-face’ categories. Here we show that microstimulation of face-selective sites, but not other sites, strongly biased the monkeys' decisions towards the face category. The magnitude of the effect depended upon the degree of face selectivity of the stimulation site, the size of the stimulated cluster of face-selective neurons, and the exact timing of microstimulation. Our results establish a causal relationship between the activity of face-selective neurons and face perception.

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Figure 1: Visual stimuli and event timing.
Figure 2: Effect of microstimulation of two representative face-selective neural clusters in IT cortex.
Figure 3: Correlation between face selectivity of stimulated sites and the behavioural impact of microstimulation.
Figure 4: Effect of stimulus selectivity of neighbouring cortical sites on microstimulation results.

References

  1. Tanaka, K. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109–139 (1996)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  3. Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051–2062 (1984)

    CAS  Article  Google Scholar 

  4. 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)

    CAS  Article  Google Scholar 

  5. Rolls, E. T. Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. Hum. Neurobiol. 3, 209–222 (1984)

    CAS  PubMed  Google Scholar 

  6. Gross, C. G. Processing the facial image: a brief history. Am. Psychol. 60, 755–763 (2005)

    Article  Google Scholar 

  7. Salzman, C. D., Murasugi, C. M., Britten, K. H. & Newsome, W. T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992)

    CAS  Article  Google Scholar 

  8. Romo, R., Hernandez, A., Zainos, A. & Salinas, E. Somatosensory discrimination based on cortical microstimulation. Nature 392, 387–390 (1998)

    ADS  CAS  Article  Google Scholar 

  9. Romo, R. & Salinas, E. Sensing and deciding in the somatosensory system. Curr. Opin. Neurobiol. 9, 487–493 (1999)

    CAS  Article  Google Scholar 

  10. Cohen, M. R. & Newsome, W. T. What electrical microstimulation has revealed about the neural basis of cognition. Curr. Opin. Neurobiol. 14, 169–177 (2004)

    CAS  Article  Google Scholar 

  11. Stoney, S. D. Jr, Thompson, W. D. & Asanuma, H. Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J. Neurophysiol. 31, 659–669 (1968)

    Article  Google Scholar 

  12. Asanuma, H., Arnold, A. & Zarzecki, P. Further study on the excitation of pyramidal tract cells by intracortical microstimulation. Exp. Brain Res. 26, 443–461 (1976)

    CAS  Article  Google Scholar 

  13. Tolias, A. S. et al. Mapping cortical activity elicited with electrical microstimulation using FMRI in the macaque. Neuron 48, 901–911 (2005)

    CAS  Article  Google Scholar 

  14. Nichols, M. J. & Newsome, W. T. Middle temporal visual area microstimulation influences veridical judgments of motion direction. J. Neurosci. 22, 9530–9540 (2002)

    CAS  Article  Google Scholar 

  15. DeAngelis, G. C. & Newsome, W. T. Perceptual “read-out” of conjoined direction and disparity maps in extrastriate area MT. PLoS Biol. 2, E77 (2004)

    Article  PubMed Central  Google Scholar 

  16. Perrett, D. I., Hietanen, J. K., Oram, M. W. & Benson, P. J. Organization and functions of cells responsive to faces in the temporal cortex. Phil. Trans. R. Soc. Lond. B 335, 23–30 (1992)

    ADS  CAS  Article  Google Scholar 

  17. 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)

    CAS  Article  Google Scholar 

  18. Zangenehpour, S. & Chaudhuri, A. Patchy organization and asymmetric distribution of the neural correlates of face processing in monkey inferotemporal cortex. Curr. Biol. 15, 993–1005 (2005)

    CAS  Article  Google Scholar 

  19. Salzman, C. D., Britten, K. H. & Newsome, W. T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990); Erratum. Nature 346, 589 (1990)

    ADS  CAS  Article  Google Scholar 

  20. Moore, T. & Armstrong, K. M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003)

    ADS  CAS  Article  Google Scholar 

  21. 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)

    CAS  Article  Google Scholar 

  22. 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)

    ADS  CAS  Article  Google Scholar 

  23. Kiani, R., Esteky, H. & Tanaka, K. Differences in onset latency of macaque inferotemporal neural responses to primate and non-primate faces. J. Neurophysiol. 94, 1587–1596 (2005)

    Article  Google Scholar 

  24. Horel, J. A., Pytko-Joiner, D. E., Voytko, M. L. & Salsbury, K. The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav. Brain Res. 23, 29–42 (1987)

    CAS  Article  Google Scholar 

  25. Buffalo, E. A. et al. Dissociation between the effects of damage to perirhinal cortex and area TE. Learn. Mem. 6, 572–599 (1999)

    CAS  Article  PubMed Central  Google Scholar 

  26. Tovee, M. J., Rolls, E. T., Treves, A. & Bellis, R. P. Information encoding and the responses of single neurons in the primate temporal visual cortex. J. Neurophysiol. 70, 640–654 (1993)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  28. Foldiak, P., Xiao, D., Keysers, C., Edwards, R. & Perrett, D. I. Rapid serial visual presentation for the determination of neural selectivity in area STSa. Prog. Brain Res. 144, 107–116 (2004)

    Article  Google Scholar 

  29. Green, D. M. & Swets, J. A. Signal Detection Theory and Psychophysics (Peninsula Publishing, Los Altos, California, 1988)

    Google Scholar 

  30. Meeker, W. Q. & Escobar, L. A. Teaching about approximate confidence regions based on maximum likelihood estimation. Am. Stat. 49, 48–53 (1995)

    Google Scholar 

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Acknowledgements

We thank S.-M. Noorbakhsh for technical assistance, and Y. Najian for training one of the monkeys. We also thank W. T. Newsome, M. N. Shadlen and N. Kanwisher for comments on the manuscript.

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Correspondence to Hossein Esteky.

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

Supplementary information

Supplementary Figure 1

Examples of shift in psychometric functions due to microstimulation. (PDF 217 kb)

Supplementary Note 1

This file contains the legend to Supplementary Figure 1. (DOC 20 kb)

Supplementary Table 1

Summary table of the fit parameters obtained from the data collected from each monkey. (DOC 32 kb)

Supplementary Note 2

This file contains the legend to Supplementary Table 1. (DOC 22 kb)

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Afraz, SR., Kiani, R. & Esteky, H. Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695 (2006). https://doi.org/10.1038/nature04982

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