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Effects of foveal prestriate and inferotemporal lesions on visual discrimination by rhesus monkeys

Summary

Ablation of inferotemporal cortex in monkeys impairs visual discrimination learning, and inferotemporal cortex receives visual information from striate cortex by way of the circumstriate belt. Yet most previous studies have failed to find any discrimination impairment after partial ablations of the circumstriate belt.

In this experiment severe impairments in post-operative acquisition and retention of visual discrimination problems were found after lesions of “foveal prestriate cortex”, i.e. the portion of the circumstriate belt which receives a projection from the cortical representation of the fovea in striate cortex and which lies, largely buried, in the ventrolateral portion of prestriate cortex. Although foveal prestriate lesions produced a greater impairment on individual pattern discrimination tasks than inferotemporal lesions, the opposite was true of concurrent visual discrimination tasks in which several different pairs of discriminanda are presented in each testing session until the animal learns to discriminate every pair.

The results are related to a two-stage model of discrimination learning and it is suggested that foveal prestriate lesions impair visual attention or perception, whereas inferotemporal lesions disturb the associative or mnemonic stage of visual discrimination learning.

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References

  1. Bower, G.H., Trebasso, T.: Attention in learning. New York: Wiley 1968.

  2. Butter, C.M., Gekoski, W.L.: Alterations in pattern equivalence following inferotemporal and lateral striate lesions in rhesus monkeys. J. comp. physiol. Psychol. 61, 309–312 (1966).

  3. Chow, K.L.: Effects of partial extirpation of posterior association cortex on visually mediated behavior in monkeys. Comp. Psychol. Monogr. 20, 187–217 (1951).

  4. Cowey, A.: Projection of the retina onto striate and prestriate cortex in the squirrel monkey, Saimiri sciureus. J. Neurophysiol. 27, 366–393 (1964).

  5. —: Perimetric study of visual field defects in monkeys after cortical and retinal ablations. Quart. J. exp. Psychol. 19, 232–245 (1967).

  6. — Weiskrantz, L.: A perimetric study of visual field defects in monkeys. Quart. J. exp. Psychol. 15, 91–115 (1963).

  7. —: A comparison of the effects of inferotemporal and striate cortex lesions on the visual behaviour of rhesus monkeys. Quart. J. exp. Psychol. 19, 246–253 (1967).

  8. Cragg, B.G., Ainsworth, A.: The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. Vision Res. 9, 737–747 (1969).

  9. Ettlinger, G.: Visual discrimination with a single manipulandum following temporal ablations in the monkey. Quart. J. exp. Psychol. 11, 164–174 (1959).

  10. Evarts, E.V.: Effects of ablation of prestriate cortex on auditory-visual association in monkey. J. Neurophysiol. 15, 191–200 (1952).

  11. Gross, C.G.: Visual functions of inferotemporal cortex. In: Handbook of Sensory Physiology, Vol. 7, Part 3. Ed. by R. Jung. Berlin-Heidelberg-New York: Springer 1970 [In press].

  12. — Bender, D.B., Rocha-Miranda, C.E.: Visual receptive fields of neurons in inferotemporal cortex of the monkey. Science 166, 1303–1305 (1969).

  13. Hubel, D.H., Wiesel, T.N.: Receptive fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).

  14. Iwai, E., Mishkin, M.: Two visual foci in the temporal lobe of monkey. Japan-U.S. Joint Seminar on Neurophysiological Basis of Learning and Behavior. Kyoto, Japan, 1968.

  15. —: Further evidence on the locus of the visual area in the temporal lobe of the monkey. Exp. Neurol. 25, 585–594 (1969).

  16. Krechevski, I.: A study of the continuity of the problem-solving process. Psychol. Rev. 45, 107–133 (1938).

  17. Kuypers, H.G.J.M., Szwarcbart, M.A., Mishkin, M., Rosvold, H.E.: Occipitotemporal cortico-cortical connections in the rhesus monkey. Exp. Neurol. 11, 245–262 (1965).

  18. Lashley, K.S.: The mechanism of vision. XVIII. Effects of destroying the visual ‘associative areas’ of the monkey. Genet. Psychol. Monogr. 37, 107–166 (1948).

  19. Lovejoy, E.: Attention in discrimination learning. London: Holden-Day 1968.

  20. Mackintosh, N.J.: Selective attention in animal discrimination learning. Psychol. Bull. 64, 124–150 (1965).

  21. Mishkin, M.: Visual mechanisms beyond the striate cortex, pp. 93–119. In: Frontiers in physiological psychology. Ed. by R.W. Russell. New York: Academic Press 1966.

  22. Olszewski, J.: The thalamus of Macaca mulatta. Basel, Switzerland: Karger 1952.

  23. Pribram, K.H., Spinelli, D.N., Reitz, S.L.: The effects of radical disconnexion of occipital and temporal cortex on visual behaviour of monkeys. Brain 92, 301–312 (1969).

  24. Riopelle, A.J., Harlow, H.F., Settlage, P.H., Ades, H.W.: Performance of normal and operated monkeys on visual learning tests. J. comp. physiol. Psychol. 44, 283–289 (1951).

  25. Sutherland, N.S.: Stimulus analyzing mechanisms, pp. 575–609. In: Proceedings of a symposium on the mechanism of thought processes. London: Her Majesty's Stationery Office 1959.

  26. —: The learning of discriminations by animals. Endeavour 23, 148–152 (1964).

  27. Teuber, H.-L., Battersby, W.S., Bender, M.B.: Visual field defects after penetrating missile wounds of the brain. Cambridge/Mass.: Harvard University Press 1960.

  28. Von Bonin, G., Bailey, P.: The neocortex of Macaca mulatta. Urbana/Ill.: University of Illinois Press 1947.

  29. Wilson, W.A., Mishkin, M.: Comparison of the effects of inferotemporal and lateral occipital lesion on visually guided behavior in monkeys. J. comp. physiol. Psychol. 52, 10–17 (1959).

  30. Zeki, S.M.: The secondary visual areas of the monkey. Brain Res. 13, 197–226 (1969a).

  31. —: Representation of central visual fields in prestriate cortex of monkey. Brain Res. 14, 271–291 (1969b).

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Additional information

This work was supported by National Institute of Mental Health Grant MH-14471, National Science Foundation Grant GB-6999 and United Cerebral Palsy Research Grant R/213/67. For providing travel expenses to the United States A. Cowey wishes to thank the H.E. Durham Fund of King's College, Cambridge, and the Royal Society. The authors are particularly indebted to D.B. Bender for advice and technical assistance. We wish to thank Dr. Mortimer Mishkin for sharing with us his ideas, enthusiasm and unpublished data.

The terminology for the subdivisions of the non-striate visual areas of the occipital and temporal lobes of the monkey is still rather confusing. This is hardly surprising, for the subdivision of these areas on cytoarchitectonic grounds by different authorities is contradictory and the study of the properties of single units in these areas has only begun. Although the recent demonstrations by Zeki (1969b) and Cragg and Ainsworth (1969) that lateral striate cortex has two topographic and a third non-topographic projection onto prestriate cortex is a major step forward, the exact boundaries of these projections and their detailed relations to the various cytoarchitectonic subdivisions and subdivisions based on electrophysiological data are not yet entirely clear. Since the terminology used in behavioural studies of lesions of the non-striate visual areas is also inconsistent, it may be helpful to explain the terminology we have used in this report.

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Cowey, A., Gross, C.G. Effects of foveal prestriate and inferotemporal lesions on visual discrimination by rhesus monkeys. Exp Brain Res 11, 128–144 (1970). https://doi.org/10.1007/BF00234318

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Key Words

  • Monkeys
  • Visual discrimination
  • Temporal lobe
  • Visual cortex