Conditioning pp 363-373 | Cite as

Neuronal Mechanisms Underlying the Formation and Disconnection of Associations Between Visual Stimuli and Reinforcement in Primates

  • Edmund T. Rolls
Part of the Advances in Behavioral Biology book series (ABBI, volume 26)

Summary

Damage to the temporal lobe neocortex or to the amygdala impairs the ability of primates to perform tasks which require the formation of learned associations between complex visual stimuli and reward or punishment. Analysis of the responses of single neurons in the anatomically connected sequence inferior temporal visual cortex / amygdala / hypothalamus in the monkey showed that neuronal responses to visual stimuli were not related in ‘the inferior temporal cortex to whether the stimuli were associated with reinforcement, were partly related to this in some amygdaloid neurons, and were related to reinforcement in a population of hypothalamic neurons. Damage to the primate orbitofrontal cortex impairs the performance of tasks which require the disconnection of associations between stimuli and reinforcement. Neuronal responses recorded in this region were related for example to whether particular visual stimuli had been reinforced previously, or for different subsets of neurons to whether reward or punishment had been obtained, or reward had been omitted. These findings thus provide evidence on how associations are formed and broken between stimuli normally of importance to primates and reinforcement, and indicate that the formation and disconnection are separable processes.

Keywords

Visual Stimulus Neuronal Response Orbitofrontal Cortex Visual Discrimination Lateral Hypothalamus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Akert, K., Gruesen, R. A., Woolsey, C. N., and Meyer, D. R., 1961, Kluver-Bucy syndrome in monkeys with neocortical ablations of temporal lobe, Brain, 84: 480–98.PubMedCrossRefGoogle Scholar
  2. Burton, M. J., Rolls, E. T. and Mora, F., 1976, Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food. Exptl. Neurol., 51: 668–77.CrossRefGoogle Scholar
  3. Butter, C. M., 1969, Perseveration in extinction and in discrimination reversal tasks following selective prefrontal ablations in Macaca mulatta, Physiol. Behay., 4: 163–71.CrossRefGoogle Scholar
  4. Divac, I., 1975, Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res., 93: 385–98.PubMedCrossRefGoogle Scholar
  5. Fuster, J. M., 1980, “The Prefrontal Cortex”, Raven Press, New York.Google Scholar
  6. Gross, C. G., Bender, D. B. and Gerstein, G. L., 1979, Activity of inferior temporal neurons in behaving monkeys,Neuropsychologia, 17: 215–29.Google Scholar
  7. Herzog,A.G. and Van Hoesen,G.W., 1976, Temporal neocortical afferent connections to the amygdala in the rhesus monkey, Brain Res., 115: 57–69.CrossRefGoogle Scholar
  8. Iversen, S.D. and Mishkin, M., 1970, Perseverative interference in monkey following selective lesions of the inferior prefrontal convexity. Exp. Brain Res., 11: 376–86.Google Scholar
  9. Jarvis, C. D. and Mishkin, M., 1977, Responses of cells in the inferior temporal cortex of monkeys during visual discrimination reversals. Soc. Neurosci. Abstr., 3: 1794.Google Scholar
  10. Jones,B. and Mishkin,M., 1972, Limbic lesions and the problem of stimulus-reinforcement associations. Exptl. Neurol., 36: 362–77.CrossRefGoogle Scholar
  11. Kievit, J. and Kuypers, H. G. J. M. frontal 1975, Subcortical afferents to the lobe in the rhesus monkey studied by means of peroxidase transport, Brain Res., retrograde horseradish 85: 261–6.Google Scholar
  12. Kluver, H. and Bucy, P. C., 1939, Preliminary analysis of functions of the temporal lobes in monkeys. Arch. Neurol. Psychiatr., 42: 979–1000.CrossRefGoogle Scholar
  13. Mora, F., Rolls, E. T. and Burton, M. J., 1976, Modulation during learning of the responses of neurons in the hypothalamus to the sight of food, Exptl. Neurol., 53: 508–19.CrossRefGoogle Scholar
  14. Nauta, W. J. H., 1961, Fiber degeneration following lesions of the amygdaloid complex in the monkey. J.Anat., 95: 515–31.PubMedGoogle Scholar
  15. Oakley, D. A., 1981, Brain mechanisms of mammalian memory, Brit. Med. Bull., 37: 175–180.PubMedGoogle Scholar
  16. Ridley, R. M., Hester, N. S. and Ettlinger, G., 1977, Stimulus-and response-dependent units from the occipital and temporal lobes of the unanaesthetized monkey performing learnt visual tasks. Exp. Brain Res., 27: 539–52.PubMedCrossRefGoogle Scholar
  17. Rolls, E. T., 1981a, Processing beyond the inferior temporal visual cortex related to feeding, memory, and striatal function. Ch. 16, pp. 241–69 in “Brain Mechanisms of Sensation”, Y.Katsuki, R.Norgren and M.Sato, eds., Wiley, New York.Google Scholar
  18. Rolls, E. T., 1981b, Central nervous mechanisms related to feeding and appetite, Brit. Med. Bull., 37: 131–4.Google Scholar
  19. Rolls, E. T., Burton, M. J. and Mora, F., 1976, Hypothalamic neuronal responses associated with the sight of food, Brain Res., 111: 53–66.PubMedCrossRefGoogle Scholar
  20. Rolls, E. T., Judge, S. J. and Sanghera, M. K., 1977, Activity of neurons in the inferotemporal cortex of the alert monkey. Brain Res., 130: 229–38.PubMedCrossRefGoogle Scholar
  21. Rolls, E. T., Sanghera, M. K. and Roper-Hall, A., 1979, The latency of activation of neurons in the lateral hypothalamus and substantia innominata during feeding in the monkey. Brain Res., 164: 121–35.PubMedCrossRefGoogle Scholar
  22. Rolls, E. T., Burton, M. J. and Mora, F., 1980, Neurophysiological analysis of brain-stimulation reward in the monkey, Brain Res., 194: 339–57.PubMedCrossRefGoogle Scholar
  23. Rosenkilde, C. E., 1979, Functional heterogeneity of the prefrontal cortex in the monkey: a review. Behay. Neural Biol., 25: 301–45.CrossRefGoogle Scholar
  24. Sanghera, M. K., Rolls, E. T. and Roper-Hall, A., 1979, Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exptl. Neurol., 63: 610–26.CrossRefGoogle Scholar
  25. Saper, C. B., Loewy, A. D., Swanson, L. W. and Cowan, W. M., 1976, Direct hypothalamo-autonomic connections. Brain Res., 117: 305–12.PubMedCrossRefGoogle Scholar
  26. Saper, C. B., Swanson, L. W. and Cowan, W. M., 1979, An autoradiographie study of the efferent connections of the lateral hypothalamic area in the rat. J. Comp. Neurol., 183: 689–706.PubMedCrossRefGoogle Scholar
  27. Sato, T., Kawamura, T., and E. Iwai, 1980, Responsiveness of inferotemporal single units to visual pattern stimuli in monkeys performing discrimination. Exp. Brain Res., 38: 313–9.PubMedCrossRefGoogle Scholar
  28. Tanaka, D., 1973, Effects of selective prefrontal decortication on escape behavior in the monkey. Brain Res., 53: 161–73.PubMedCrossRefGoogle Scholar
  29. Teuber, H.-L., 1964, The riddle of frontal lobe function in man. Pp. 410–77 in “The Frontal Granular Cortex and Behavior”, eds. J.M.Warren and K.Akert, McGraw-Hill, New York.Google Scholar
  30. Thorpe, S. J., Maddison, S. and Rolls, E. T., 1979, Single unit activity in the orbitofrontal cortex of the behaving monkey. Neurosci. Lett., S3: S77.Google Scholar
  31. Weiskrantz, L., 1956, Behavioral changes associated with ablation of the amygdaloid complex in monkeys, J. Comp. Physiol. Psychol., 49: 381–91.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1982

Authors and Affiliations

  • Edmund T. Rolls
    • 1
  1. 1.Oxford UniversityDepartment of Experimental PsychologyOxfordUK

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