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Neuronal Activity in the Inferomedial Temporal Cortex Compared with That in the Hippocampal Formation

Implications for Amnesia of Medial Temporal Lobe Origin
  • F. A. W. Wilson
  • M. W. Brown
  • I. P. Riches

Abstract

Numerous studies have reported that bilateral lesions of the medial temporal lobes cause enduring anterograde amnesia in man (Scoville and Milner, 1957; Victor et al., 1961; De-Jong et al., 1969; Van Buren and Borke, 1972). There are two major and as yet unsolved issues concerning the nature of this amnesia: the structures within the medial temporal lobes that are crucial for memory function and the precise processes that are impaired by the lesions. Published accounts of the temporal lobe damage accompanying the amnesia generally describe lesions of the hippocampus, adjacent temporal cortex, and the amygdala in varying degrees and combinations. Zola-Morgan et al. (1986) have reported a patient (case R.B.) with complete bilateral destruction of region CA1 of the hippocampus. This patient was amnesic, but differed from the patient H.M. (Scoville and Millner, 1957) in two major respects: first, the hippocampal lesions of H.M. were subtotal, sparing the posterior third of the hippocampus; second, H.M.’s impairment was much more severe than R.B. As noted by Squire (1987), damage to the medial temporal cortex exacerbates memory impairments. Thus, it is not clear what the specific contributions of the hippocampus, the amygdala, and the adjacent temporal cortex are to memory and related mechanisms.

Keywords

Recognition Memory Temporal Cortex Basal Forebrain Medial Temporal Lobe Hippocampal Formation 
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References

  1. Adey, W. R., Dunlop, C. W., and Hendrix, C. E., 1960, Hippocampal slow waves: Distribution and phase relationships in the course of approach learning, Arch. Neurol. 3: 74–90.PubMedCrossRefGoogle Scholar
  2. Aggleton, J. P., and Mishkin, M., 1983, Memory impairments following restricted medial thalamic lesions in monkeys, Exp. Brain Res. 52: 199–209.PubMedCrossRefGoogle Scholar
  3. Aggleton, J. P., and Passingham, R. E., 1981, Stereotaxic surgery under x-ray guidance in the rhesus monkey, with special reference to the amgydala, Exp. Brain Res. 44: 271–276.PubMedCrossRefGoogle Scholar
  4. Aggleton, J. P., Burton, M. J., and Passingham, R. E., 1980, Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta), Brain Res. 190: 347–368.PubMedCrossRefGoogle Scholar
  5. Aggleton, J. P., Desimone, R., and Mishkin, M., 1986, The origin, course and termination of the hippocampothalamic projections in the macaque, J. Comp. Neurol. 243: 409–421.PubMedCrossRefGoogle Scholar
  6. Aigner, T., Mitchell, S., Aggleton, J., DeLong, M., Struble, R., Wenk G., Price, D., and Mishkin, M., 1984, Recognition deficit in monkeys following neurotoxic lesions of the basal forebrain, Soc. Neurosci. Abstr. 10: 116. 11.Google Scholar
  7. Arnolds, D. E. A. T., Lopes Da Silva, F. H., Aitink, J. W., Kamp, A., and Boeijinga, P., 1980, The spectral properties of hippocampal EEG related to behaviour in man, EET Clin. Neurophysiol. 50: 324–328.Google Scholar
  8. Baylis, G. C., and Rolls, E. T., 1983, Responses of neurons in the inferior temporal visual cortex in short and long term memory tasks, Soc. Neurosci. Abstr. 9: 12. 2.Google Scholar
  9. Biber, C., Butters, N., Rosen, J., Gerstman, L., and Mattis, S., 1981, Encoding strategies and recognition of faces by alcoholic Korsakoff and other brain-damaged patients, J. Clin. Neuropsychol. 3: 315–350.CrossRefGoogle Scholar
  10. Brown, M. W., 1982, Effect of context on the response of single units recorded from the hippocampal region of behaviorally trained monkeys, in: Neuronal Plasticity and Memory Formation ( C. Ajmone Marsan and H. Matthies, eds.), Raven Press, New York, pp. 557–573.Google Scholar
  11. Brown, M. W., and Leendertz, J. A., 1979, A pulse-shape discriminator for action potential, J. Physiol. (Lond.) 298: 17–18 P.Google Scholar
  12. Brun, A., and Englund, E., 1981, Regional pattern of degeneration in Alzheimer’s disease: Neuronal loss and histopathological grading, Histopathology 5: 549–564.PubMedCrossRefGoogle Scholar
  13. Buerger, A. A., Gross, C. G., and Rocha-Miranda, C. E., 1974, Effects of ventral putamen lesions on discrimination learning by monkeys, J. Comp. Physiol. Psychol. 86: 440–446.PubMedCrossRefGoogle Scholar
  14. Caan, W., Perrett, D. I., and Rolls, E. T., 1984, Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum, Brain Res. 290: 53–65.PubMedCrossRefGoogle Scholar
  15. Cermak, L. S., Talbot, N., Chandler, K., and Wolbarst, L. R., 1985, The perceptual priming phenomenon in amnesia, Neuropsychologia 23: 615–622.PubMedCrossRefGoogle Scholar
  16. Damasio, A. R., Graff-Radford, N. R., Eslinger, P. J., Damasio, H., and Kassel, N., 1985, Amnesia following basal forebrain lesions, Arch. Neurol. 42: 263–271.PubMedCrossRefGoogle Scholar
  17. DeJong, R. N., Itabashi, H. H., and Olson, J. R., 1969, Memory loss due to hippocampal lesions, Arch. Neurol. 20: 339–348.PubMedCrossRefGoogle Scholar
  18. Desimone, R., and Gross, C. G., 1979, Visual areas in the temporal cortex of the macaque, Brain Res. 178: 363–380.PubMedCrossRefGoogle Scholar
  19. Divac, I., Rosvold, H. E., and Szwarcbart, M. K, 1967, Behavioural effects of selective ablation of the caudate nucleus, J. Comp. Physiol. Psychol. 63: 184–190.PubMedCrossRefGoogle Scholar
  20. Flicker, C., Ferris, S. H., Crook, T., Bartus, R. T., and Reisberg, B., 1985, Cognitive function in normal aging and early dementia, in: Senile Dementia of the Alzheimer Type ( J. Traber and W. H. Gispen, eds.), Springer-Verlag, Berlin, pp. 2–37.CrossRefGoogle Scholar
  21. Friedman, H. M., and Allen, N., 1969, Chronic effects of complete limbic lobe distruction in man, Neurology (Minneap.) 19: 679–689.CrossRefGoogle Scholar
  22. Gaffan, D., 1974, Recognition impaired and association intact in the memory of monkeys after transection of the fornix, J. Comp. Physiol. Psychol. 86: 1100–1109.PubMedCrossRefGoogle Scholar
  23. Gaffan, D., 1977, Monkeys’ recognition memory for complex pictures and the effect of fomix transection, Q. J. Exp. Psychol. 29: 505–514.PubMedCrossRefGoogle Scholar
  24. Gaffan, D., 1985, Hippocampus: Memory, habit and voluntary movement, Phil. Trans. R. Soc. Lond. [Biol.] 308: 87–99.CrossRefGoogle Scholar
  25. Gaffan, D., Saunders, R. C., Gaffan, E. A., Harrison, S., Shields, C., and Owen, M. J., 1984, Effects of fornix transection upon associative memory in monkeys: Role of the hippocampus in learned action, Q. J. Exp. Psychol. 36B: 173–221.Google Scholar
  26. Gascon, G. G., and Gilles, F., 1973, Limbic dementia, J. Neurol. Neurosurg. Psychiatry 36: 421–430.PubMedCrossRefGoogle Scholar
  27. Gross, C. G., 1972, Visual functions of inferotemporal cortex, in: Handbook of Sensory Physiology, Vol. VIII/3B ( R. Jung, ed.), Springer-Verlag, Berlin, pp. 451–482.Google Scholar
  28. Halgren, E., Babb, T. L., and Crandall, P. H., 1978, Activity of human hippocampal formation and amygdale neurons during memory testing, Electroencephalogr. Clin. Neurophysiol. 45: 585–601.PubMedCrossRefGoogle Scholar
  29. Horel, J. A., 1978, The neuroanatomy of amnesia. A critique of the hippocampal memory hypothesis, Brain 101: 403–445.PubMedCrossRefGoogle Scholar
  30. Horel, J. A., and Pytko, D. E., 1982, Behavioural effect of local cooling in temporal lobe of monkeys, J. Neurophysiol. 47: 11–22.PubMedGoogle Scholar
  31. Huppert, F. A., and Piercy, M., 1978, The role of trace strength in recency and frequency judgements by amnesic and control subjects, Q. J. Exp. Psychol. 30: 347–354.PubMedCrossRefGoogle Scholar
  32. Jacobs, B. L., and McGinty, D. J., 1972, Participation of the amygdala in complex stimulus recognition and behavioural inhibition: Evidence from unit studies, Brain Res. 36: 431–436.PubMedCrossRefGoogle Scholar
  33. Jacoby, L. L., and Witherspoon, D., 1982, Remembering without awareness, Can. J. Psychol. 36: 300–324.CrossRefGoogle Scholar
  34. Jones, B., and Mishkin, M., 1972, Limbic lesions and the problem of stimulus—reinforcement associations, Exp. Neurol. 36: 362–377.PubMedCrossRefGoogle Scholar
  35. Jones, E. G., and Powell, T. P. S., 1970, An anatomical study of the converging sensory pathways within the cerebral cortex of the monkey, Brain 93: 793–820.PubMedCrossRefGoogle Scholar
  36. Leichnetz, G. R., and Astruc, J., 1976, The efferent projections of the medial prefrontal cortex in the squirrel monkey (Saimiri Sciureus), Brain Res. 109: 455–472.PubMedCrossRefGoogle Scholar
  37. Leonard, C. M., Rolls, E. T., Wilson, F. A. W., and Baylis, G. C., 1985, Neurons in the amygdala of the monkey with responses selective for faces, Behay. Brain Res. 15: 159–176.CrossRefGoogle Scholar
  38. Mahut, H., 1972, A selective spatial deficit in monkeys after transection of the fornix, Neuropsychologia 10: 65–74.PubMedCrossRefGoogle Scholar
  39. Mahut, H., Zola Morgan, S., and Moss, M., 1982, Hippocampal resections impair associative learning and recognition memory in the monkey, J. Neurosci. 2: 1214–1229.PubMedGoogle Scholar
  40. McLardy, M., 1970, Memory function in hippocampal gyri but not in hippocampi, Int. J. Neurol. 1:113–118. Mesulam, M.-M., and Mufson, E. J., 1982, Insula of the Old World monkey. 1: Architectonics in the insuloorbito-temporal component of the paralimbic brain, J. Comp. Neurol. 212: 1–22.Google Scholar
  41. Mesulam, M.-M., and Mufson, E. J., 1984, Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey, Brain 107: 257–274.CrossRefGoogle Scholar
  42. Mesulam, M.-M., Rosen, A. D., and Mufson, E. J., 1984, Regional variations in cortical cholinergic innervation: Chemoarchitectonics of acetylcholinesterase-containing fibres in the macaque brain, Brain Res. 311: 245–258.PubMedCrossRefGoogle Scholar
  43. Milner, B., 1970, Memory and the medial temporal regions of the brain, in: Biology of Memory ( K. H. Pribram and D. E. Broadbent, eds.), Academic Press, New York, pp. 29–50.Google Scholar
  44. Mishkin, M., 1978, Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus, Nature 273: 297–299.PubMedCrossRefGoogle Scholar
  45. Mishkin, M., 1982, A memory system in the monkey, Phil. Trans. R. Soc. Lond. [Biol.] 298:85–95. Mishkin, M., and Bachevalier, J., 1983, Object recognition impaired by ventromedial but not dorsolateral prefrontal cortical lesions in monkeys, Soc. Neurosci. Abstr. 9: 12. 13.Google Scholar
  46. Mishkin, M., and Delacour, J., 1975, An analysis of short-term visual memory in the monkey, J. Exp. Psychol. Anim. Behay. Proc. 1: 326–334.CrossRefGoogle Scholar
  47. Murray, E. A., and Mishkin, M., 1984, Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys, J. Neurosci. 4: 2565–2580.PubMedGoogle Scholar
  48. Murray, E. A., Bachevalier, J., and Mishkin, M., 1985, Rhinal cortex: A third temporal-lobe component of the limbic memory system, Soc. Neurosci. Abstr. 11: 140. 13.Google Scholar
  49. O’Keefe, J., and Bouma, H., 1969, Complex sensory properties of certain amygdala units in the freely moving cat, Exp. Neurol. 23: 384–398.PubMedCrossRefGoogle Scholar
  50. O’Keefe, J., and Nadel, L., 1978, The Hippocampus as a Cognitive Map, Clarendon Press, Oxford.Google Scholar
  51. Owen, M. J., and Butler, S. R., 1981, Amnesia after transection of the fornix in moneys: Long-term memory impaired, short-term memory intact, Behay. Brain Res. 3: 115–123.CrossRefGoogle Scholar
  52. Parkinson, J. K., and Mishkin, M., 1982, A selective mnemonic role for the hippocampus in monkeys: Memory for the location of objects, Soc. Neurosci. Abstr. 8: 11. 7.Google Scholar
  53. Pearson, R. C. A., Esiri, M. M., Hioms, R. W., Wilcocks, G. K., and Powell, T. P. S., 1985, Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer disease, Proc. Natl. Acad. Sci U.S.A. 82: 4531–4534.PubMedCrossRefGoogle Scholar
  54. Pribram, K. H., Wilson, W. A., Jr., and Connors, J., 1962, Effects of lesions of the medial forebrain on alternation behaviour of rhesus monkeys, Exp. Neurol. 6: 36–47.PubMedCrossRefGoogle Scholar
  55. Ranck, J. B., Jr., 1973, Studies on single neurones in dorsal hippocampal formation and septum in unrestrained rats. Part 1. Behavioural correlates and firing repertoires, Exp. Neurol. 414: 461–531.Google Scholar
  56. Ringo, J. L., and Doty, R. W., 1985, A macaque remembers pictures briefly viewed six months earlier, Behay. Brain Res. 18: 289–294.CrossRefGoogle Scholar
  57. Rolls, E. T., Perrett, D. I., Caan, A. W., and Wilson, F. A. W., 1982, Neuronal responses related to visual recognition, Brain 105: 611–646.PubMedCrossRefGoogle Scholar
  58. Russchen, F. T., Amaral, D. G., and Price, J. L., 1985, The afferent connections of the substantia innominata in the monkey, Macaca fasicularis, J. Comp. Neurol. 242: 1–27.PubMedCrossRefGoogle Scholar
  59. Sawa, M., and Delgado, J. M. R., 1963, Amygdala unitary activity in the unrestrained cat, Electroencephalogr. Clin. Neurophysiol. 15: 637–560.PubMedCrossRefGoogle Scholar
  60. Scoville, W. B., and Milner, B., 1957, Loss of recent memory after bilateral hippocampal lesions, J. Neurol. Neurosurg. Psychiatry 20: 11–22.PubMedCrossRefGoogle Scholar
  61. Seltzer, B., and Pandya, D. N., 1978, Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey, Brain Res. 149: 1–24.PubMedCrossRefGoogle Scholar
  62. Sidman, M., Stoddard, L. T., and Mohr, J. P., 1968, Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions, Neuropsychologia 6: 245–254.CrossRefGoogle Scholar
  63. Spiegler, B. J., and Mishkin, M., 1981, Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus—reward associations, Behay. Brain Res. 3: 303–317.CrossRefGoogle Scholar
  64. Squire, L. R., and Moore, R. Y., 1979, Dorsal thalamic lesion in a noted case of chronic memory dysfuntion, Ann. Neurol. 6: 503–506.PubMedCrossRefGoogle Scholar
  65. Squire, L. R., 1987, Memory and Death, Oxford University Press, New York.Google Scholar
  66. Steward, O., and Scoville, S. A., 1976, Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat, J. Comp. Neurol. 169: 347–370.PubMedCrossRefGoogle Scholar
  67. Thompson, R. F., and Spencer, W. A., 1966, Habituation: A model phenomenon for the study of neuronal substrates of behaviour, Psychol. Rev. 173: 16–43.CrossRefGoogle Scholar
  68. Van Buren, J. M., and Borke, R. C., 1972, The mesial temporal substratum of memory: Anatomical studies in three individuals, Brain 95: 599–632.PubMedCrossRefGoogle Scholar
  69. Vanderwolf, C. H., Kramis, R., Gilespi, L. A., and Bland, B. H. 1975, Hippocampal rhythmic slow activity and neocortical low-voltage fast activity: Relations to behaviour, in: The Hippocampus, Vol. 2 ( R. L. Isaacson and K. H. Pribram, eds., Plenum Press, New York, pp. 101–128.Google Scholar
  70. Van Hoesen, G. W., and Pandya, D., 1975, Some connections of the entorhinal (area 28) and perirhinal cortices of the rhesus monkey. 1. Temporal lobe afferents, Brain Res. 95: 1–24.PubMedCrossRefGoogle Scholar
  71. Van Hoesen, G. W., Yeterian, E. H., and Lavizzo-Mourey, R., 1981, Widespread corticostriate projections from temporal cortex of the rhesus monkey, J. Comp. Neurol. 199: 205–219.PubMedCrossRefGoogle Scholar
  72. Victor, M., Angevine, J. B., Mancall, E. L., and Fisher, C. M., 1961, Memory loss with lesions of hippocampal formation, Arch. Neurol. 5: 244–263.PubMedCrossRefGoogle Scholar
  73. Wallesch, C. W., Kornhuber, H. H., Kollner, C., Haas, H. C., and Hufnagl, J. M., 1983, Language and cognitive deficits resulting from medial and dorsolateral frontal lobe lesions, Arch. Psychiatr. Nervenkr. 233: 279–296.PubMedCrossRefGoogle Scholar
  74. Warrington, E. K., 1974, Deficient recognition memory in organic amnesia, Cortex 10: 289–291.PubMedCrossRefGoogle Scholar
  75. Warrington, E. K., and Weiskrantz, L., 1974, The effect of prior learning on subsequent retention in amnesic patients, Neuropsychologia 12: 419–428.PubMedCrossRefGoogle Scholar
  76. Warrington, E. K., and Weiskrantz, L., 1979, Conditioning in amnesic patients, Neuropsychologia 17: 187194.Google Scholar
  77. Watanabe, T., and Niki, H., 1985, Hippocampal unit activity and delayed response in the monkey, Brain Res. 325: 241–254.PubMedCrossRefGoogle Scholar
  78. Weiskrantz, L., 1956, Behavioural changes associated with ablation of the amygdaloid complex in monkeys, J. Comp. Physiol. Psychol. 49: 381–391.PubMedCrossRefGoogle Scholar
  79. Weiskrantz, L., 1982, Comparative aspects of studies of amnesia, Phil. Trans. R. Soc. Lond. [Biol.] 298: 97–109.CrossRefGoogle Scholar
  80. Whitehouse, P. J., Price, A. W., Clark, A. W., Coyle, J. T., and DeLong, M. R., 1981, Alzheimer’s disease: Evidence for a selective loss of cholinergic neurons in the nucleus basalis, Ann. Neurol. 10: 122–126.PubMedCrossRefGoogle Scholar
  81. Whitlock, D. G., and Nauta, W. J. H., 1956, Subcortical projections from the temporal neocortex in Macaca mulatta, J. Comp. Neurol. 106: 184–207.CrossRefGoogle Scholar
  82. Wilson, F. A. W., 1985, Neuronal Activity Related to Novelty, Familiarity and Reinforcement, D.Phil. Thesis, Oxford University.Google Scholar
  83. Wilson, F. A. W., and Rolls, E. T., 1985, Reinforcement-related unit activity in basal forebrain and amygdala, Soc. Neurosci. Abstr. 11: 160. 1.Google Scholar
  84. Wilson, F. A. W., Rolls, E. T., Yaxley, S., Thorpe, S. J., Williams, G. V., and Simpson, S. J., 1984, Responses of neurons in the basal forebrain of the behaving monkey, Soc. Neurosci. Abstr. 10: 37. 8.Google Scholar
  85. Wilson, F. A. W., Brown, M. W., and Riches, I. P., 1986, Response-related neuronal activity in the primate hippocampal formation, Neurosci. Lett. Suppl. 24: S29.Google Scholar
  86. Winocur, G., Oxbury, S., Roberts, R., Agnetti, A., and Davis, C., 1984, Amnesia in a patient with bilateral lesions to the thalamus, Neuropsychologia 22: 123–143.PubMedCrossRefGoogle Scholar
  87. Zola-Morgan, S., and Squire, L. R., 1984, Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills, J. Neurosci. 4: 1072–1085.PubMedGoogle Scholar
  88. Zola-Morgan, S., and Squire, L. R., 1985, Medial temporal lesions impair memory on a wide variety of tasks sensitive to human amnesia, Behay. Neurosci. 99: 22–34.CrossRefGoogle Scholar
  89. Zola-Morgan, S., Squire, L. R., and Amaral, D. G., 1984, Performance of monkeys with separate and combined lesions of the hippocampus and amygdala on delayed non-matching to sample, Soc. Neurosci. Abstr. 10: 116. 7.Google Scholar
  90. Zola-Morgan, S., Squire, L. R., and Amaral, D., 1986, Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to the CA 1 field of the hippocampus, J. Neurosci. 6: 2950–2967.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1988

Authors and Affiliations

  • F. A. W. Wilson
    • 1
  • M. W. Brown
    • 2
  • I. P. Riches
    • 2
  1. 1.Section of Neuroanatomy, School of MedicineYale UniversityNew HavenUSA
  2. 2.Department of Anatomy, The Medical SchoolUniversity of BristolBristolEngland

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