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Impact of learning on representation of parts and wholes in monkey inferotemporal cortex

Abstract

Here we investigated the impact of visual discrimination training on neuronal responses to parts of images and to whole images in inferotemporal (IT) cortex. Monkeys were trained to discriminate among 'baton' stimuli consisting of discrete top and bottom parts joined by a vertical stem. With separate features at each end, we were able to manipulate the two parts of each baton independently. After training the monkeys, we used single-cell recording to compare neuronal responses to learned and unlearned batons. Responses to learned batons, though not enhanced in strength, were enhanced in selectivity for both individual parts and for whole batons. Whole-baton selectivity arose from a form of conjunctive encoding whereby two parts together exerted a greater influence on neuronal activity than predicted by the additive influence of each part considered individually. These results indicate a possible neural mechanism for holistic or configural effects in expert versus novice observers.

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Figure 1: Baton stimuli and recording location.
Figure 2: Response to the best learned baton plotted against response to the best unlearned baton.
Figure 3: Selectivity was enhanced for learned as compared to unlearned batons.
Figure 4: Selectivity for the individual parts of learned batons was enhanced relative to selectivity for individual parts of unlearned batons.
Figure 5: Learning enhanced the tendency of neurons to respond selectively to just one baton within a tetrad.

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References

  1. Wallis, G. & Bülthoff, H. Learning to recognize objects. Trends Cogn. Sci. 3, 22–31 (1999).

    Article  CAS  Google Scholar 

  2. Tanaka, J. & Gauthier, I. in Psychology of Learning and Motivation Vol. 36 (eds. Goldstone, R. L., Schyns, P. G. & Medin, D. L.) 83–125 (Academic Press, New York, 1997).

    Google Scholar 

  3. Sheinberg, D.L. & Logothetis, N.K. in Perceptual Learning (eds. Fahle, M. & Poggio, T.) 95–124 (MIT Press, Cambridge, MA, 2002).

    Google Scholar 

  4. Hasegawa, I. & Miyashita, Y. Categorizing the world: expert neurons look into key features. Nat. Neurosci. 5, 90–91 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. 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 

  8. 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 

  9. Li, L., Miller, E.K. & Desimone, R. The representation of stimulus familiarity in anterior inferior temporal cortex. J. Neurophysiol. 69, 1918–1929 (1993).

    Article  CAS  Google Scholar 

  10. Xiang, J.-Z. & Brown, M.W. Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37, 657–676 (1998).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  12. 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 

  13. Messinger, A., Squire, L.R., Zola, S.M. & Albright, T.D. Neuronal representations of stimulus associations develop in the temporal lobe during learning. Proc. Nat. Acad. Sci. USA 98, 12239–12244 (2001).

    Article  CAS  Google Scholar 

  14. Logothetis, N.K. & Pauls, J. Psychophysical and physiological evidence for viewer-centered object representations in the primate. Cereb. Cortex 3, 270–288 (1995).

    Article  Google Scholar 

  15. Logothetis, N.K., Pauls, J. & Poggio, T. Shape representation in the inferior temporal cortex of monkeys. Curr. Biol. 5, 552–563 (1995).

    Article  CAS  Google Scholar 

  16. Erickson, C.A., Jagadeesh, B. & Desimone, R. Clustering of perirhinal neurons with similar properties following visual experience in adult monkeys. Nat. Neurosci. 3, 1143–1148 (2000).

    Article  CAS  Google Scholar 

  17. Vogels, R. & Orban, G.A. Does practice in orientation discrimination lead to changes in the response properties of macaque inferior temporal neurons? Eur. J. Neurosci. 6, 1680–1690 (1994).

    Article  CAS  Google Scholar 

  18. 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 

  19. Sakai, K. & Miyashita, Y. Neuronal tuning to learned complex forms in vision. Neuroreport 5, 829–832 (1994).

    Article  CAS  Google Scholar 

  20. Miyashita, Y., Date, A. & Okuno, H. Configurational encoding of complex visual forms by single neurons of monkey temporal cortex. Neuropsychologia 31, 1119–1131 (1993).

    Article  CAS  Google Scholar 

  21. Gauthier, I. & Tarr, M.J. Unraveling mechanisms for expert object recognition: bridging brain activity and behavior. J. Exp. Psychol. Hum. Percept. Perform. 28, 431–446 (2002).

    Article  Google Scholar 

  22. Tanaka, J.W. & Farah, M.J. in Analytic and Holistic Processes in Perception of Faces, Objects and Scenes (eds. Peterson, M. A. & Rhodes, G.) (Oxford Univ. Press, New York, in press).

  23. Murray, E.A. & Bussey, T.J. Perceptual-mnemonic functions of the perirhinal cortex. Trends Cogn. Sci. 3, 142–151 (1999).

    Article  CAS  Google Scholar 

  24. Bussey, T.J. & Saksida, L.M. The organization of visual object representations: a connectionist model of effects of lesions in perirhinal cortex. Eur. J. Neurosci. 15, 355–364 (2002).

    Article  Google Scholar 

  25. Bussey, T.J., Saksida, L.M. & Murray, E.A. Perirhinal cortex resolves feature ambiguity in complex visual discriminations. Eur. J. Neurosci. 15, 365–374 (2002).

    Article  Google Scholar 

  26. Perrett, D.I., Rolls, E.T. & Caan, W. Visual neurons responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329–342 (1982).

    Article  CAS  Google Scholar 

  27. 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 

  28. 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 

  29. 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 

  30. Tsunoda, T., Yamane, Y., Nishizaki, M. & Tanifuji, M. Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns. Nat. Neurosci. 4, 832–838 (2001).

    Article  CAS  Google Scholar 

  31. Desimone, R. Neural mechanisms for visual memory and their role in attention. Proc. Natl. Acad. Sci. USA 93, 13494–13499 (1996).

    Article  CAS  Google Scholar 

  32. Op De Beeck, H. & Vogels, R. Spatial sensitivity of macaque inferior temporal neurons. J. Comp. Neurol. 426, 505–518 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Desimone, R. Visual attention mediated by biased competition in extrastriate visual cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1245–1255 (1998).

    Article  CAS  Google Scholar 

  35. Op de Beeck, H., Wagemans, J. & Vogels, R. Inferotemporal neurons represent low-dimensional configurations of parameterized shapes. Nat. Neurosci. 4, 1244–1252 (2001).

    Article  CAS  Google Scholar 

  36. Xiang, J.-Z. & Brown, M.W. Differential neuronal responsiveness in primate perirhinal cortex and hippocampal formation during performance of a conditional visual discrimination task. Eur. J. Neurosci. 11, 3715–3724 (1999).

    Article  CAS  Google Scholar 

  37. Vogels, R. Categorization of complex visual images by rhesus monkeys. Part 2: single-cell study. Eur. J. Neurosci. 11, 1239–1255 (1999).

    Article  CAS  Google Scholar 

  38. Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291, 312–316 (2001).

    Article  CAS  Google Scholar 

  39. 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 

  40. Goldstone, R.L. Unitization during category learning. J. Exp. Psychol. Hum. Percept. Perform. 26, 86–112 (2000).

    Article  CAS  Google Scholar 

  41. Goldstone, R.L. Perceptual learning. Annu. Rev. Psychol. 49, 585–612 (1998).

    Article  CAS  Google Scholar 

  42. Zar, J.H. Biostatistical Analysis 4th edn. (Prentice Hall, Upper Saddle River, New Jersey, 1999).

    Google Scholar 

  43. Pasupathy, A. & Connor, C.E. Shape representation in area V4: position-specific tuning for boundary conformation. J. Neurophysiol. 86, 2505–2519 (2001).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by National Institute of Health grant RO1 EY11831. We thank K. Medler and K. McCracken for technical assistance.

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Correspondence to Chris I. Baker.

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Baker, C., Behrmann, M. & Olson, C. Impact of learning on representation of parts and wholes in monkey inferotemporal cortex. Nat Neurosci 5, 1210–1216 (2002). https://doi.org/10.1038/nn960

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