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Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex

Abstract

Categorization and fine discrimination are two different functions in visual perception, and we can switch between these two functions depending on the situation or task demands. To explore how visual cortical neurons behave in such situations, we recorded the activities of color-selective neurons in the inferior temporal (IT) cortex of two monkeys trained to perform a color categorization task, a color discrimination task and a simple fixation task. Many IT neurons changed their activity depending upon the task, although color selectivity was well conserved. A majority of neurons showed stronger responses during the categorization task. Moreover, for the population of IT neurons as a whole, signals contributing to performing the categorization task were enhanced. These results imply that judgment of color category by color-selective IT neurons is facilitated during the categorization task and suppressed during the discrimination task as a consequence of task-dependent modulation of their activities.

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Figure 1: Experimental paradigm, visual stimuli, cortical area explored in this study and task performances.
Figure 2: Responses of two representative color-selective neurons that showed task dependency.
Figure 3: Distribution of the magnitudes of the task effect and the time course of the task dependency.
Figure 4: Triangular plot showing the relative strength of the neuronal activity during the fixation (top corner), categorization (bottom right corner) and discrimination (bottom left corner) tasks.
Figure 5: Red-green color selectivity in the categorization and discrimination tasks.
Figure 6: Stability of the color-selectivity of neurons that showed task-dependent differences in their response magnitudes.
Figure 7: Distribution of the categorization indices and comparison between tasks.

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References

  1. Fuster, J.M. Executive frontal functions. Exp. Brain Res. 133, 66–70 (2000).

    Article  CAS  Google Scholar 

  2. Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  Google Scholar 

  3. White, I.M. & Wise, S.P. Rule-dependent neuronal activity in the prefrontal cortex. Exp. Brain Res. 126, 315–335 (1999).

    Article  CAS  Google Scholar 

  4. Asaad, W.F., Rainer, G. & Miller, E.K. Task-specific neural activity in the primate prefrontal cortex. J. Neurophysiol. 84, 451–459 (2000).

    Article  CAS  Google Scholar 

  5. Wallis, J.D., Anderson, K.C. & Miller, E.K. Single neurons in prefrontal cortex encode abstract rules. Nature 411, 953–956 (2001).

    Article  CAS  Google Scholar 

  6. Sakagami, M. & Niki, H. Encoding of behavioral significance of visual stimuli by primate prefrontal neurons: relation to relevant task conditions. Exp. Brain Res. 97, 423–436 (1994).

    Article  CAS  Google Scholar 

  7. Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).

    Article  CAS  Google Scholar 

  8. Luck, S.J., Chelazzi, L., Hillyard, S.A. & Desimone, R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24–42 (1997).

    Article  CAS  Google Scholar 

  9. Connor, C.E., Preddie, D.C., Gallant, J.L. & Van Essen, D.C. Spatial attention effects in macaque area V4. J. Neurosci. 17, 3201–3214 (1997).

    Article  CAS  Google Scholar 

  10. McAdams, C.J. & Maunsell, J.H. 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 

  11. Reynolds, J.H., Pasternak, T. & Desimone, R. Attention increases sensitivity of V4 neurons. Neuron 26, 703–714 (2000).

    Article  CAS  Google Scholar 

  12. Motter, B.C. Neural correlates of attentive selection for color or luminance in extrastriate area V4. J. Neurosci. 14, 2178–2189 (1994).

    Article  CAS  Google Scholar 

  13. McAdams, C.J. & Maunsell, J.H. Attention to both space and feature modulates neuronal responses in macaque area V4. J. Neurophysiol. 83, 1751–1755 (2000).

    Article  CAS  Google Scholar 

  14. Ogawa, T. & Komatsu, H. Target selection in area V4 during a multidimensional visual search task. J. Neurosci. 24, 6371–6382 (2004).

    Article  CAS  Google Scholar 

  15. Ungerleider, L.G. & Mishkin, M. Two cortical visual systems. In Analysis of Visual Behavior (eds. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W.) 549–586 (MIT Press, Cambridge, Massachusetts, USA, 1982).

    Google Scholar 

  16. Webster, M.J., Bachevalier, J. & Ungerleider, L.G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb. Cortex 4, 470–483 (1994).

    Article  CAS  Google Scholar 

  17. Komatsu, H., Ideura, Y., Kaji, S. & Yamane, S. Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey. J. Neurosci. 12, 408–424 (1992).

    Article  CAS  Google Scholar 

  18. Takechi, H. et al. Mapping of cortical areas involved in color vision in non-human primates. Neurosci. Lett. 230, 17–20 (1997).

    Article  CAS  Google Scholar 

  19. Tootell, R.B., Nelissen, K., Vanduffel, W. & Orban, G.A. Search for color 'center(s)' in macaque visual cortex. Cereb. Cortex 14, 353–363 (2004).

    Article  Google Scholar 

  20. Heywood, C.A., Gaffan, D. & Cowey, A. Cerebral achromatopsia in monkeys. Eur. J. Neurosci. 7, 1064–1073 (1995).

    Article  CAS  Google Scholar 

  21. Buckley, M.J., Gaffan, D. & Murray, E.A. Functional double dissociation between two inferior temporal cortical areas: perirhinal cortex versus middle temporal gyrus. J. Neurophysiol. 77, 587–598 (1997).

    Article  CAS  Google Scholar 

  22. Huxlin, K.R., Saunders, R.C., Marchionini, D., Pham, H.A. & Merigan, W.H. Perceptual deficits after lesions of inferotemporal cortex in macaques. Cereb. Cortex 10, 671–683 (2000).

    Article  CAS  Google Scholar 

  23. Chelazzi, L., Miller, E.K., Duncan, J. & Desimone, R. A neural basis for visual search in inferior temporal cortex. Nature 363, 345–347 (1993).

    Article  CAS  Google Scholar 

  24. Richmond, B.J. & Sato, T. Enhancement of inferior temporal neurons during visual discrimination. J. Neurophysiol. 58, 1292–1306 (1987).

    Article  CAS  Google Scholar 

  25. Miller, E.K., Li, L. & Desimone, R. A neural mechanism for working and recognition memory in inferior temporal cortex. Science 254, 1377–1379 (1991).

    Article  CAS  Google Scholar 

  26. Mikami, A. & Kubota, K. Inferotemporal neuron activities and color discrimination with delay. Brain Res. 182, 65–78 (1980).

    Article  CAS  Google Scholar 

  27. Baylis, G.C. & Rolls, E.T. Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks. Exp. Brain Res. 65, 614–622 (1987).

    Article  CAS  Google Scholar 

  28. Eskandar, E.N., Richmond, B.J. & Optican, L.M. Role of inferior temporal neurons in visual memory. I. Temporal encoding of information about visual images, recalled images, and behavioral context. J. Neurophysiol. 68, 1277–1295 (1992).

    Article  CAS  Google Scholar 

  29. Vogels, R., Sary, G. & Orban, G.A. How task-related are the responses of inferior temporal neurons? Vis. Neurosci. 12, 207–214 (1995).

    Article  CAS  Google Scholar 

  30. Naya, Y., Sakai, K. & Miyashita, Y. Activity of primate inferotemporal neurons related to a sought target in pair-association task. Proc. Natl Acad. Sci. USA 93, 2664–2669 (1996).

    Article  CAS  Google Scholar 

  31. Miyashita, Y. Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature 335, 817–820 (1988).

    Article  CAS  Google Scholar 

  32. Takeda, M., Naya, Y., Fujimichi, R., Takeuchi, D. & Miyashita, Y. Active maintenance of associative mnemonic signal in monkey inferior temporal cortex. Neuron 48, 839–848 (2005).

    Article  CAS  Google Scholar 

  33. Vogels, R. & Orban, G.A. Activity of inferior temporal neurons during orientation discrimination with successively presented gratings. J. Neurophysiol. 71, 1428–1451 (1994).

    Article  CAS  Google Scholar 

  34. Hung, C.P., Kreiman, G., Poggio, T. & DiCarlo, J.J. Fast readout of object identity from macaque inferior temporal cortex. Science 310, 863–866 (2005).

    Article  CAS  Google Scholar 

  35. Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. A comparison of primate prefrontal and inferior temporal cortices during visual categorization. J. Neurosci. 23, 5235–5246 (2003).

    Article  CAS  Google Scholar 

  36. Suzuki, W., Matsumoto, K. & Tanaka, K. Neuronal responses to object images in the macaque inferotemporal cortex at different stimulus discrimination levels. J. Neurosci. 26, 10524–10535 (2006).

    Article  CAS  Google Scholar 

  37. Dean, P. Effects of inferotemporal lesions on the behavior of monkeys. Psychol. Bull. 83, 41–71 (1976).

    Article  CAS  Google Scholar 

  38. Kaiser, P.K. & Boynton, R.M. Human Color Vision (Optical Society of America, Washington, DC, 1996).

    Google Scholar 

  39. Bornstein, M.H. Perceptual categories in vision and audition. In Categorical Perception: The Groundwork of Cognition (ed. Harnad, S.R.) 287–300 (Cambridge Univ. Press, New York, 1987).

    Google Scholar 

  40. 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 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  44. Riesenhuber, M. & Poggio, T. Models of object recognition. Nat. Neurosci. 3 (suppl.): 1199–1204 (2000).

    Article  CAS  Google Scholar 

  45. 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  CAS  Google Scholar 

  46. Judge, S.J., Richmond, B.J. & Chu, F.C. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 20, 535–538 (1980).

    Article  CAS  Google Scholar 

  47. Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. Visual categorization and the primate prefrontal cortex: neurophysiology and behavior. J. Neurophysiol. 88, 929–941 (2002).

    Article  Google Scholar 

Download references

Acknowledgements

We thank M. Ito and N. Goda for comments on the manuscript and M. Togawa for technical assistance. This work was supported by the Grant-in-Aid for Scientific Research (B) and for Scientific Research on Priority Areas 〈System study on higher-order brain functions〉 (17022040) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Correspondence to Hidehiko Komatsu.

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Supplementary information

Supplementary Fig. 1

Color selectivity and shape selectivity of the representative cells whose activities are shown in Figure 2. (PDF 18 kb)

Supplementary Fig. 2

Reproducibility of the task effect across separate blocks. (PDF 16 kb)

Supplementary Figure 3

Temporal profile of the task effect and color selectivity affecting the activities of all 124 neurons. (PDF 16 kb)

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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). https://doi.org/10.1038/nn1823

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