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Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns

Abstract

Intrinsic signal imaging from inferotemporal (IT) cortex, a visual area essential for object perception and recognition, revealed that visually presented objects activated patches in a distributed manner. When visual features of these objects were partially removed, the simplified stimuli activated only a subset of the patches elicited by the originals. This result, in conjunction with extracellular recording, suggests that an object is represented by a combination of cortical columns, each of which represents a visual feature (feature column). Simplification of an object occasionally caused the appearance of columns that were not active when viewing the more complex form. Thus, not all the columns related to a particular feature were necessarily activated by the original objects. Taken together, these results suggest that objects may be represented not only by simply combining feature columns but also by using a variety of combinations of active and inactive columns for individual features.

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Figure 1: Intrinsic signal imaging detects local modulation of light absorption changes in area TE.
Figure 2: Relationship between intrinsic signals and spike activity in area TE.
Figure 3: Representation of complex object images and simplifications of them in area TE.
Figure 4: Visual responsiveness of representative cells in spots A–D in Fig. 3d.
Figure 5: The optimal visual stimuli of 25 cells in spots A to D in Fig. 3d.
Figure 6: The distribution pattern of active spots elicited by two original object images (stimulus 1 and 3) and a simplified image of stimulus 1 (stimulus 2).
Figure 7: Visual responsiveness of representative cells in spots A and B in Fig. 6.

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References

  1. Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. Visual properties of neurons in inferotemporal cortex of the Macaque. J. Neurophysiol . 35, 96–111 (1972).

    Article  CAS  Google Scholar 

  2. 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 

  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).

    Article  CAS  Google Scholar 

  4. Tanaka, K., Saito, H., 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 

  5. Kobatake, E. & Tanaka, K. Neuronal selectivities to complex object features in the ventral pathway of the macaque cerebral cortex. J. Neurophysiol. 71, 856–867 (1994).

    Article  CAS  Google Scholar 

  6. Ts'o, D. Y., Frostig, R. D., Lieke, E. E. & Grinvald, A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417–420 (1990).

    Article  CAS  Google Scholar 

  7. Blasdel, G. G. Orientation selectivity, preference, and continuity in monkey striate cortex. J. Neurosci. 12, 3139–3161 (1992).

    Article  CAS  Google Scholar 

  8. Das, A. & Gilbert, C. D. Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex. Nature 375, 780–784 (1995).

    Article  CAS  Google Scholar 

  9. Roe, A. W. & Ts'o, D. Y. Visual topography in primate V2: multiple representation across functional stripes. J. Neurosci. 15, 3689–3715 (1995).

    Article  CAS  Google Scholar 

  10. Ghose, G. M. & Ts'o, D. Y. Form processing modules in primate area V4. J. Neurophysiol. 77, 2191–2196 (1997).

    Article  CAS  Google Scholar 

  11. Malonek, D., Tootell, R. B. & Grinvald, A. Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT. Proc. R. Soc. Lond. B Biol. Sci. 258, 109–119 (1994).

    Article  CAS  Google Scholar 

  12. 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 

  13. Wang, G., Tanifuji, M. & Tanaka, K. Functional architecture in monkey inferotemporal cortex revealed by in vivo optical imaging. Neurosci. Res. 32, 33–46 (1998).

    Article  CAS  Google Scholar 

  14. Uchida, N., Takahashi, Y. K., Tanifuji, M. & Mori, K. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat. Neurosci. 3, 1035–1043 (2000).

    Article  CAS  Google Scholar 

  15. Gochin, P. M., Miller, E. K., Gross, C. G. & Gerstein, G. L. Functional interactions among neurons in inferior temporal cortex of the awake macaque. Exp. Brain. Res. 84, 505–516 (1991).

    Article  CAS  Google Scholar 

  16. 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 

  17. Marr, D. & Nishihara, H. K. Representation and recognition of the spatial organization of three-dimensional shapes. Proc. R. Soc. Lond. B Biol. Sci. 200, 269–294 (1978).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  19. Ullman, S. Computation of pattern invariance in brain-like structures. Neural Net. 12, 1021–1036 (1999).

    Article  CAS  Google Scholar 

  20. Edelman, S., Grill-Spector, K., Kushnir, T. & Malach, R. Toward direct visualization of the internal shape representation space by fMRI. Psychobiology 26, 309–321 (1998).

    Google Scholar 

  21. Ishai, A., Ungerleider, L. G., Martin, A., Schouten, J. L. & Haxby, J. V. Distributed representation of objects in the human ventral visual pathway. Proc. Natl. Acad. Sci. USA 96, 9379–9384 (1999).

    Article  CAS  Google Scholar 

  22. Wang, Y., Fujita, I. & Murayama, Y. Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex. Nat. Neurosci. 3, 807–813 (2000).

    Article  CAS  Google Scholar 

  23. 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 

  24. Yamane, S., Kaji, S. & Kawano, K. What facial features activate face neurons in the inferotemporal cortex of the monkey? Exp. Brain Res. 73, 209–214 (1988).

    Article  CAS  Google Scholar 

  25. Hasselmo, M. E., Rolls, E. T., Baylis, G. C. & Nalwa, V. Object-centered encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey. Exp. Brain Res. 75, 417–429 (1989).

    Article  CAS  Google Scholar 

  26. Sakai, K. & Miyashita, Y. Neural organization for the long-term memory of paired associates. Nature 354, 152–155 (1991).

    Article  CAS  Google Scholar 

  27. Erickson, C. A. & Desimone, R. Responses of macaque perirhinal neurons during and after visual stimulus association learning. J. Neurosci. 19, 10404–10416 (1999).

    Article  CAS  Google Scholar 

  28. Shtoyerman, E., Arieli, A., Slovin, H., Vanzetta, I. & Grinvald, A. Long-term optical imaging and spectroscopy reveal mechanisms underlying the intrinsic signal and stability of cortical maps in V1 of behaving monkeys. J. Neurosci. 20, 8111–8121 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank K.S. Rockland, R. Kado, K. Tanaka, and S. Edelman for comments on the manuscript, M. Fukuda for technical assistance throughout the experiments, and M. Matsumoto for modifying the data acquisition program. This project was partly supported by Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Corporation.

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Correspondence to Manabu Tanifuji.

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Tsunoda, K., Yamane, Y., Nishizaki, M. et al. Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns. Nat Neurosci 4, 832–838 (2001). https://doi.org/10.1038/90547

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