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Form representation in monkey inferotemporal cortex is virtually unaltered by free viewing

Abstract

How are objects represented in the brain during natural behavior? Visual object recognition in primates is thought to depend on the inferotemporal cortex (IT). In most neurophysiological studies of IT, monkeys hold their direction of gaze fixed while isolated visual stimuli are presented (controlled viewing). However, during natural behavior, primates visually explore cluttered environments by changing gaze direction several times each second (free viewing). We examined the effect of free viewing on IT neuronal responses in monkeys engaged in a form-recognition task. By making small, real-time stimulus adjustments, we produced nearly identically retinal stimulation during controlled and free viewing. Nearly 90% of neuronal responses were unaffected by free viewing, and average stimulus selectivity was unchanged. Thus, neuronal representations that likely underlie form recognition are virtually unaltered by free viewing.

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Figure 1: Visual stimuli and recognition task.
Figure 2: The four main task conditions.
Figure 3: Task differences in gaze behavior and control of retinal stimulation.
Figure 4: Response of a target-selective IT neuron to each target stimulus in each task condition.
Figure 5: Effect of viewing condition on single neuronal responses.
Figure 6: Average target-sensitivity functions during controlled and free viewing.
Figure 7: Time course of the average response during controlled and free viewing.

References

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

    CAS  Article  Google Scholar 

  2. Miyashita, Y. Inferior temporal cortex: where visual perception meets memory. Annu. Rev. Neurosci. 16, 245–263 (1993).

    CAS  Article  Google Scholar 

  3. Booth, M. C. A. & Rolls, E. T. View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. Cereb. Cortex 8, 510– 523 (1998).

    CAS  Article  Google Scholar 

  4. 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).

    CAS  Article  Google Scholar 

  5. Missal, M., Vogels, R., Li, C. & Orban, G. A. Shape interactions in macaque inferior temporal neurons. J. Neurophysiol. 82, 131–142 (1999).

    CAS  Article  Google Scholar 

  6. Rollenhagen, J. E. & Olson, C. R. Mirror-image confusion in single neurons of the macaque inferotemporal cortex. Science 287, 1506–1508 ( 2000).

    CAS  Article  Google Scholar 

  7. Gibson, J. R. & Maunsell, J. H. R. The sensory modality specificity of neural activity related to memory in visual cortex. J. Neurophysiol. 78, 1263–1275 ( 1997).

    CAS  Article  Google Scholar 

  8. Findlay, J. Active vision: Visual activity in everyday life. Curr. Biol. 8, R640–R642 (1998).

    CAS  Article  Google Scholar 

  9. Motter, B. C. & Belky, E. J. The zone of focal attention during active visual search. Vision Res. 38, 1007 –1022 (1998).

    CAS  Article  Google Scholar 

  10. Sommer, M. A. Express saccades elicited during visual scan in the monkey. Vision Res. 34, 2023–2038 ( 1994).

    CAS  Article  Google Scholar 

  11. Burman, D. D. & Segraves, M. A. Primate frontal eye field activity during natural scanning eye movements. J. Neurophysiol. 71, 1266–1271 (1994).

    CAS  Article  Google Scholar 

  12. Ballard, D. Animate vision. Artificial Intelligence 48, 57–86 (1991).

    Article  Google Scholar 

  13. Dawkins, M. S. & Woodington, A. Pattern recognition and active vision in chickens. Nature 403, 652–655 (2000).

    CAS  Article  Google Scholar 

  14. Gallant, J. L., Connor, C. E. & Van Essen, D. C. Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing. Neuroreport 9, 2153–2158 ( 1998).

    CAS  Article  Google Scholar 

  15. Livingstone, M. S., Freeman, D. C. & Hubel, D. H. Visual responses in V1 of freely viewing monkeys . Cold Spring Harb. Symp. Quant. Biol. 61, 27–37 (1996).

    CAS  Article  Google Scholar 

  16. Vinje, W. E. & Gallant, J. L. Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273–1276 (2000).

    CAS  Article  Google Scholar 

  17. Guido, W. & Weyand, T. Burst responses in thalamic relay cells of the awake behaving cat. J. Neurophysiol. 74 , 1782–1786 (1995).

    CAS  Article  Google Scholar 

  18. Judge, S. J., Wurtz, R. H. & Richmond, B. J. Vision during saccadic eye movements. I. Visual interactions in striate cortex. J. Neurophysiol. 43, 1133–1155 (1980).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  20. Liu, Z. & Richmond, B. J. Response differences in monkey TE and perirhinal cortex: stimulus association related to reward schedules . J. Neurophysiol. 83, 1677– 1692 (2000).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  22. Gochin, P. M., Colombo, M., Dorfman, G. A., Gerstein, G. L. & Gross, C. G. Neural ensembly coding in inferior temporal cortex. J. Neurophysiol. 71, 2325 –2337 (1994).

    CAS  Article  Google Scholar 

  23. Britten, K. H., Shadlen, M. N., Newsome, W. T. & Movshon, J. A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745– 4765 (1992).

    CAS  Article  Google Scholar 

  24. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 ( 1991).

    CAS  Article  Google Scholar 

  25. Ross, J., Burr, D. & Morrone, C. Suppression of the magnocellular pathway during saccades . Behav. Brain Res. 80, 1– 8 (1996).

    CAS  Article  Google Scholar 

  26. Diamond, M. R., Ross, J. & Morrone, M. C. Extraretinal control of saccadic suppression. J. Neurosci. 20, 3449–3455 (2000).

    CAS  Article  Google Scholar 

  27. Castet, E. & Masson, G. S. Motion perception during saccadic eye movements. Nat. Neurosci. 3, 177– 183 (2000).

    CAS  Article  Google Scholar 

  28. Ungerleider, L. G. & Mishkin, M. in Analysis of Visual Behavior (eds. Ingle, D. J., Goodale, M. A. & Mansfield, R. J. W.) 549–585 (MIT Press, Cambridge, Massachusetts, 1982).

    Google Scholar 

  29. Maunsell, J. H. R., Nealey, T. A. & DePriest, D. D. Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. J. Neurosci. 10, 3323–3334 (1990).

    CAS  Article  Google Scholar 

  30. Colby, C. L. & Goldberg, M. E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319– 349 (1999).

    CAS  Article  Google Scholar 

  31. Ferrera, V. P., Nealey, T. A. & Maunsell, J. H. R. Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways. J. Neurosci. 14, 2080–2088 (1994).

    CAS  Article  Google Scholar 

  32. Leopold, D. A. & Logothetis, N. K. Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Exp. Brain Res. 123, 341– 345 (1998).

    CAS  Article  Google Scholar 

  33. Ringo, J. L., Sobotka, S., Diltz, M. D. & Bunce, C. M. Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. J. Neurophysiol. 71, 1285– 1288 (1994).

    CAS  Article  Google Scholar 

  34. Maunsell, J. H. R. The brain's visual world: representation of visual targets in cerebral cortex . Science 270, 764–769 (1995).

    CAS  Article  Google Scholar 

  35. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193– 222 (1995).

    CAS  Article  Google Scholar 

  36. Vega-Bermudez, F., Johnson, K. O. & Hsiao, S. S. Human tactile pattern recognition: active versus passive touch, velocity effects, patterns of confusion. J. Neurophysiol. 65, 531–546 ( 1991).

    CAS  Article  Google Scholar 

  37. Robinson, D. A. A method of measuring eye movements using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Eng. 101, 131 –145 (1963).

    Google Scholar 

  38. Bahill, A., Clark, M. & Stark, L. Glissades—eye movements generated by mismatched components of the sacadic motorneuronal control signal. Math. Biosciences 26, 303–318 ( 1975).

    Article  Google Scholar 

  39. Martinez-Conde, S., Macknik, S. L. & Hubel, D. H. Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nat. Neurosci. 3, 251–258 ( 2000).

    CAS  Article  Google Scholar 

  40. Snedecor, G. W. & Cochran, W. D. Statistical Methods (Iowa Univ. Press, Ames, Iowa, 1967).

    Google Scholar 

  41. Gur, M. & Snodderly, D. M. Studying striate cortex neurons in behaving monkeys: benefits of image stabilization. Vision Res. 27, 2081–2087 ( 1987).

    CAS  Article  Google Scholar 

  42. Baylis, G. C., Rolls, E. T. & Leonard, C. M. Functional subdivisions of the temporal lobe neocortex . J. Neurosci. 7, 330–342 (1987).

    CAS  Article  Google Scholar 

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Acknowledgements

We thank C. Boudreau, E. Cook, G. Ghose, and T. Yang for discussions on design, analysis and presentation, and D. Murray for animal husbandry. We also thank K. Johnson and D. Sparks for comments on a previous version of this manuscript. This work was supported by NIH EY05911. J.H.R.M. is an Investigator with the Howard Hughes Medical Institute.

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Correspondence to James J. DiCarlo.

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DiCarlo, J., Maunsell, J. Form representation in monkey inferotemporal cortex is virtually unaltered by free viewing. Nat Neurosci 3, 814–821 (2000). https://doi.org/10.1038/77722

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