Ontogenetic Development and Decline of Memory Functions in Nonhuman Primates

  • Jocelyne Bachevalier
  • Mortimer Mishkin


An emerging parallel view in research on ontogeny and decline of memory abilities is that mnemonic processes are differentially susceptible to age. Some behavioral memory tasks are performed normally by newborn monkeys, whereas other memory tasks are performed normally only if the animal is mature. Similarly, some memory tasks are performed normally by aged subjects while other tasks are not. Thus, it appears that the presence and absence of age-related memory abilities depend on the specific information-processing demands of the behavioral tasks used to measure memory functions. One important outcome of characterizing impaired versus preserved memory function in ontogeny or aging is the insight this information can provide concerning the neural systems that mediate age-dependent cognitive functions. Neuropsychological findings in amnesic patients and in monkeys with experimental brain damage have indicated that different brain regions appear to make rather specialized contributions to learning and memory. Accordingly, specific types of cognitive abilities in infant and aged subjects may reflect the functional status of those brain regions that mediate the component processes of memory. Based on this neuropsychological perspective, this chapter will review actual knowledge on the ability of both infant, mature, and aged monkeys to form habits and memories, two learning processes that are known to depend on separate neural circuits.


Medial Temporal Lobe Visual Recognition Amnesic Patient Inferior Temporal Cortex Aged Monkey 
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  1. Aggleton JP, Desimone R, Mishkin M (1986): The origin, course, and termination of the hippocampothalamic projections in the macaque. Journal of Comparative Neurology 243:409–421CrossRefGoogle Scholar
  2. Aggleton JP, Mishkin M (1983a): Visual recognition memory impairment following medial thalamic lesions in monkeys. Neuropsychologia 21:189–197CrossRefGoogle Scholar
  3. Aggleton JP, Mishkin M (1983b): Memory impairments following restricted medial thalamic lesions in monkeys. Experimental Brain Research 52: 199–209CrossRefGoogle Scholar
  4. Aggleton JP, Mishkin M (1984): Projections of the amygdala to the thalamus in the cynomolgus monkey. Journal of Comparative Neurology 222:56–68CrossRefGoogle Scholar
  5. Aggleton JP, Mishkin M (1985): Mammillary-body lesions and visual recognition in the monkey. Experimental Brain Research 58:190–197CrossRefGoogle Scholar
  6. Aigner T, Mitchell S, Aggleton JP, DeLong M, Struble R, Wenk G, Price D, Mishkin M (1984): Recognition deficits in monkeys following neurotoxic lesions of the basal forebrain. Society for Neuroscience Abstracts 10:386Google Scholar
  7. Alexander MP, Freedman M (1984): Amnesia after anterior communicating artery aneurysm rupture. Neurology 34:752–757Google Scholar
  8. Amaral DG (1987): Memory: anatomical organization of candidate brain regions. In: Handbook of Physiology. Section 1. The Nervous System, Mountcastle VB, Plum F, Geiser SR, eds. Bethesda: American Physiological Association, pp. 211–294Google Scholar
  9. Amaral DG, Cowan WM (1980): Subcortical afferents to the hippocampal formation in the monkey. Journal of Comparative Neurology 189:573–591CrossRefGoogle Scholar
  10. Angelergues R, Hecaen H, De Ajuriaguerra J (1955): Les troubles mentaux au cours des tumeurs du lobe frontal. Annals of Medical Psychology 113:577–642Google Scholar
  11. Arendt T, Bigl V, Arendt A, Tennstedt A (1983): Loss of neurons in the nucleus basalis of Meynert in Alzheimer’s disease, paralysis agitans, and Korsakoff’s disease. Acta Neuropathologica 61:101–108CrossRefGoogle Scholar
  12. Arnsten AFT, Goldman-Rakic PS (1985): Alpha-adrenergic mechanisms in prefrontal cortex associated with cognitive decline in aged nonhuman primates. Science 230:1273–1276CrossRefGoogle Scholar
  13. Bachevalier J (1990): Ontogenetic development of habit and memory formation in primates. In: The Development and Neural Bases of Higher Cognitive Functions, Diamond A, ed. Annals of New York Academy of Sciences 608:457–486Google Scholar
  14. Bachevalier J (1991) Cortical vs limbic immaturity: Relationship to infantile amnesia. In: Minnesota Symposium on Child Psychology: Developmental Neu-roscience, Gunnar M, Nelson CA, eds. New York: Erlbaum, 24:129–153Google Scholar
  15. Bachevalier J, Brickson M, Hagger C, Mishkin N (1990): Age and sex differences in the effects of selective temporal lobe lesion on the formation of visual discrimination habits in rhesus monkeys (Macaca mulatto). Behavioral Neuroscience 104:885–899CrossRefGoogle Scholar
  16. Bachevalier J, Hagger C, Mishkin M (1991a): Functional maturation of the occipitotemporal pathway in infant rhesus monkeys. In: Alfred Benzon Symposium 31: Brain Work and Mental Activity, Copenhagen: Munksgaard, pp. 231–240Google Scholar
  17. Bachevalier J, Landis LS, Walker LC, Brickson N, Mishkin M, Price DL, Cork LC (1991b): Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction. Neurobiology of Aging 12:99–111CrossRefGoogle Scholar
  18. Bachevalier J, Mishkin M (1984): An early and a late developing system for learning and retention in infant monkeys. Behavioral Neuroscience 98:770–778CrossRefGoogle Scholar
  19. Bachevalier J, Mishkin M (1986): Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behavioral Brain Research 20:249–261CrossRefGoogle Scholar
  20. Bachevalier J, Mishkin M (1988): Long-term effects of neonatal temporal cortical and limbic lesions on habit and memory formation in rhesus monkeys. Society for Neuroscience Abstracts 14:1Google Scholar
  21. Bachevalier J, Parkinson JK, Mishkin M (1985): Visual recognition: effects of separate vs. combined transection of fornix and amygdalofugal pathways. Experimental Brain Research 57:554–561Google Scholar
  22. Bachevalier J, Ungerleider LG, O’Neill B, Friedman DP (1986): Regional distribution of [3H]naloxone binding in the brain of a newborn rhesus monkey. Developmental Brain Research 25:302–308CrossRefGoogle Scholar
  23. Baleydier C, Mauguiere F (1980): The duality of the cingulate gyrus in monkey: neuroanatomical study and functional hypothesis. Brain 103:525–554CrossRefGoogle Scholar
  24. Bartus RT (1979): Effects of aging on visual memory, sensory processing and discrimination learning in nonhuman primate. In: Sensory Systems and Communication in the Elderly, Ordy JM, Brizzee K, eds. New York: Raven, pp. 85–144Google Scholar
  25. Battig K, Rosvold HE, Mishkin M (1960): Comparison of the effects of frontal and caudate lesions on delayed response and alternation in monkeys. Journal of Comparative Physiology and Psychology 53:400–404CrossRefGoogle Scholar
  26. Brooks DN, Baddeley AD (1976): What can amnesic patients learn? Neuropsy-chologia 14:111–122CrossRefGoogle Scholar
  27. Brozovski TJ, Brown RM, Rosvold HE, Goldman PS (1979): Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205:929–932CrossRefGoogle Scholar
  28. Buerger AA, Gross CG, Rocha-Miranda CE (1974): Effects of ventral putarnen lesions on discrimination learning by monkeys. Journal of Comparative Physiology and Psychology 86:440–446CrossRefGoogle Scholar
  29. Butters SN, Cermak LS (1980): Alcoholic Korsakoff’s Syndrome—An Information-Processing Approach to Amnesia. New York: Academic PressGoogle Scholar
  30. Candy J, Perry R, Perry E, Irving D, Blessed G, Fairnairn A and Tomlinson B (1983): Pathological changes in the nucleus of Meynert in Alzheimer’s and Parkinson’s diseases. Journal of Neurological Science 54:277–289CrossRefGoogle Scholar
  31. Cohen NJ, Squire LR (1980): Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of “knowing how” and “knowing that.” Science 210:207–209CrossRefGoogle Scholar
  32. Corkin S (1965): Tactually-guided maze learning in man: Effects of unilateral cortical excisions and bilateral hippocampal lesions. Neuropsychologic 3:339–351CrossRefGoogle Scholar
  33. Corkin S (1968): Acquisition of motor skill after bilateral medial temporal-lobe excision. Neuropsychologia 6: 255–266CrossRefGoogle Scholar
  34. Davis RT (1985): The effects of aging on the behavior of rhesus monkeys. In: Behavior and Pathology of Aging in Rhesus Monkeys. Monographs in Pri-matology Vol. 8, Davis RT, Leathers CW, eds. New York: Alan R. Liss, pp.57–82Google Scholar
  35. Divac I, Rosvold HE, Szwarcbart MK (1967): Behavioral effects of selective ablation of the caudate nucleus. Journal of Comparative Physiology and Psychology 63:184–190CrossRefGoogle Scholar
  36. Ellis RJ, Oscar-Berman M (1989): Alcoholism, aging, and functional cerebral asymmetries. Psychological Bulletin 106:128–147CrossRefGoogle Scholar
  37. Gade A (1982): Amnesia after operations on aneurysms of the anterior communicating artery. Surgical Neurology 18:46–49CrossRefGoogle Scholar
  38. Goldman PS (1975): Age, sex, and experience as related to the neural basis of cognitive development. In: Brain Mechanisms in Mental Retardation, Buch-Wald NA, Brazier MAB, eds. New York: Academic Press, pp. 379–392Google Scholar
  39. Goldman PS, Rosvold HE (1970): Localization of function within the dorsolateral prefrontal cortex of the rhesus. Experimental Neurology 27: 291–304CrossRefGoogle Scholar
  40. Goldman PS, Rosvold HE, Vest B, Galkin TW (1971): Analysis of the delayed-alternation deficit produced by dorsolateral prefrontal lesions in the rhesus monkey. Journal of Comparative Physiology and Psychology 77:212–220CrossRefGoogle Scholar
  41. Horel JA (1978): The neuroanatomy of amnesia: A critique of the hippocampal memory hypothesis. Brain 101:403–445CrossRefGoogle Scholar
  42. Korsakoff SS (1887): Disturbance of psychic function in alcoholic paralysis and its relation to the disturbance of the psychic sphere in multiple neuritis of nonalcoholic origin. Psychiatrii 4: fascicle 2Google Scholar
  43. Lilly R, Cummings JL, Benson F, Frankel M (1983): The human Klüver-Bucy syndrome. Neurology 83:1141–1145Google Scholar
  44. Mair WGP, Warrington E, Weiskrantz L (1979): Memory disorders in Korsakoff’s psychosis. A neuropathological and neuropsychological investigation of two cases. Brain 102:749–783CrossRefGoogle Scholar
  45. Malamut BL, Saunders RC, Mishkin M (1984): Monkeys with combined amyg-dalo-hippocampal lesions succeed in object discrimination learning despite 24-hour intertriai intervals. Behavioral Neuroscience 98:759–769CrossRefGoogle Scholar
  46. Mesulam M, Mufson E, Levey A, Wainer B (1983): Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata): and hypothalamus in the rhesus monkey. Journal of Comparative Neurology 214:170–197CrossRefGoogle Scholar
  47. Meunier M, Murray EA, Bachevalier J, Mishkin M (1990) Effects of perirhinal cortical lesions in visual recognition memory in rhesus monkeys. Society for Neuroscience Abstracts 16:616Google Scholar
  48. Milner B (1962): Les troubles de la mémoire accompagnant des lésions hippocam-piques bilatérales. In: Physiologie de l’hippocampe, Passouant P, ed. Paris: Centre de la Recherche Scientifique, pp. 257–272Google Scholar
  49. Milner B (1972): Disorders of learning and memory after temporal lobe lesions in man. Clinical Neurosurgery 19:421–446Google Scholar
  50. Mishkin M (1954): Visual discrimination performance following partial ablations of the temporal lobes Ventral surface vs. hippocampus. Journal of Comparative Physiology and Psychology 47:187–193CrossRefGoogle Scholar
  51. Mishkin M (1978): Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus. Nature 273:297–298CrossRefGoogle Scholar
  52. Mishkin M (1982): A memory system in the monkey. Philosophical Transactions of the Royal Society of London Series B, 298:85–95CrossRefGoogle Scholar
  53. Mishkin M, Appenzeller T (1987): The anatomy of memory. Scientific American 256:80–89CrossRefGoogle Scholar
  54. Mishkin M, Malamut BL, Bachevalier J (1984): Memories and habits: Two neural systems. In: Neurobiology of Learning and Memory, Lynch G, McGaugh L, Weinberger NM, eds. New York: Guilford, pp. 65–77Google Scholar
  55. Mishkin M, Petri HL (1984): Memories and habits: Some implications for the analysis of learning and retention. In: Neuropsychology of Memory, Butters N, Squire L, eds. New York: Guilford, pp. 287–296Google Scholar
  56. Murray EA (1991): Medial temporal lobe structures contributing of recognition memory: The amygdaloid complex versus the perirhinal cortex. In: Neurobiology of the Amygdala, Aggleton JP, ed. New York: Wiley-Liss, pp. 453–470Google Scholar
  57. Murray EA, Bachevalier J, Mishkin M (1989): Effects of rhinal cortical lesions on visual recognition memory in rhesus monkeys. Society for Neuroscience Abstracts 15:342Google Scholar
  58. Murray EA, Mishkin M (1983): Severe tactual memory deficits in monkeys after combined removal of the amygdala and hippocampus. Brain Research 270:340–344CrossRefGoogle Scholar
  59. Nauta WJH (1962): Neural associations of the amygdaloid complex in the monkey. Brain 85:505–520CrossRefGoogle Scholar
  60. O’Neill B, Friedman DP, Bachevalier J, Ungerleider LG (1986): Distribution of muscarinic cholinergic receptors in the brain of a newborn monkey. Society for Neuroscience Abstracts 12:809Google Scholar
  61. Overman WH (1991): Performance on traditional match-to-sample, nonmatch-to-sample, and object discrimination tasks by 12 to 32 month-old children: A developmental progression. In: Development and Neural Bases of Higher Cognitive Functions, Diamond A, ed. Annals of New York Academy of Sciences 608:365–390Google Scholar
  62. Passingham RE (1985): The memory of monkeys (Macaca mulatta) with lesions in prefrontal cortex. Behavioral Neuroscience 99:3–21CrossRefGoogle Scholar
  63. Penfield W, Milner B (1958): Memory deficit produced by bilateral lesions in the hippocampal zone. American Medical Association Archives of Neurology and Psychiatry 79:475–497Google Scholar
  64. Petrides M, Iversen SD (1979): Restricted posterior parietal lesions in the rhesus monkey and performance on visuospatial tasks. Brain Research 161:63–77CrossRefGoogle Scholar
  65. Phillips RR, Malamut BL, Bachevalier J, Mishkin M (1988): Dissociation of the effects of inferior temporal and limbic lesions on object discrimination learning with 24-hr intertriai intervals. Behavioral Brain Research 27:99–107CrossRefGoogle Scholar
  66. Presty SK, Bachevalier J, Walker LC, Struble RG, Price DL, Mishkin M, Cork LC (1987): Age differences in recognition memory of the rhesus monkey (Macaca mulatta). Neurobiology of Aging 8:435–440CrossRefGoogle Scholar
  67. Pribram KH, Mishkin M, Rosvold HE, Kaplan SJ (1952): Effects on delayed-response performance of lesions of dorsolateral and ventromedial frontal cortex of baboon. Journal of Comparative Physiology and Psychology 45:565–575CrossRefGoogle Scholar
  68. Provensal JC (1951): Les tumeurs frontales. Etudes anatomo-cliniques de 82 observations. Thesis, MarseilleGoogle Scholar
  69. Rapp PR, Amaral DG (1989): Evidence for task-dependent memory dysfunction in the aged monkey. Journal of Neuroscience 9:3568–3576Google Scholar
  70. Ribot T (1881): Les maladies de la mémoire. Paris: Germer-BaillereGoogle Scholar
  71. Rosenkilde CE (1979): Functional heterogeneity of the prefrontal cortex in the monkey: A review. Behavioral and Neural Biology 25:301–345CrossRefGoogle Scholar
  72. Saint-Cyr JA, Taylor AE, Lang AE (1988): Procedural learning and neostriatal dysfunction in man. Brain 111:941–959CrossRefGoogle Scholar
  73. Scoville WB, Milner B (1957): Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry 20:11–21CrossRefGoogle Scholar
  74. Spiegler BJ, Mishkin M (1981): Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations. Behavioral Brain Research 3:303–317CrossRefGoogle Scholar
  75. Squire LR (1987): Memory and Brain. New York: Oxford University PressGoogle Scholar
  76. Talland G (1965): Deranged Memory. New York: Academic PressGoogle Scholar
  77. Talland GA, Sweet WT, Ballantine HT (1967): Amnesic syndrome with anterior communicating artery aneurysm. Journal of Nervous Mental Disease 145:179–192CrossRefGoogle Scholar
  78. Tobias TJ (1975): Afférents to prefrontal cortex from the thalamic mediodorsal nucleus in the rhesus monkey. Brain Research 83:191–212CrossRefGoogle Scholar
  79. Turner B, Mishkin M, Knapp M (1980): Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. Journal of Comparative Neurology 191:515–543CrossRefGoogle Scholar
  80. Van Hoesen GW, Pandya DN (1975): Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkeys: I. Temporal lobe afférents. Brain Research 95:1–24CrossRefGoogle Scholar
  81. Victor M, Adams RD, Collins GH (1971): The Wernicke-Korsakoff Syndrome. Philadelphia: DavisGoogle Scholar
  82. Wang J, Aigner T, Mishkin M (1990): Effects of neostriatal lesions on visual habit formation in rhesus monkeys. Society for Neuroscience Abstracts 16:617Google Scholar
  83. Warrington E, Weiskrantz L (1968): New method of testing long-term retention with special reference to amnesic patients. Nature (Lond) 217:972–974CrossRefGoogle Scholar
  84. Whitehouse P, Price DL, Struble R, Clark A, Coyle J, DeLong M (1982): Alzheimer’s disease and senile dementia: Loss of neurons in the basal forebrain. Science 215:1237–1239CrossRefGoogle Scholar
  85. Whitty CWM, Levin W (1960): A Korsakoff’s syndrome in the postcingulectomy confusional state. Brain 83:648–653CrossRefGoogle Scholar
  86. Zola-Morgan S, Squire LR (1985a): Complementary approaches to the study of memory: Human amnesia and animal models. In: Memory Systems of the Brain: Animal and Human Cognitive Processes, Weinberger NW, McGaugh JL, Lynch L, eds. New York: Guilford, pp. 463–477Google Scholar
  87. Zola-Morgan S, Squire LR (1985b): Amnesia in monkeys after lesions of the mediodorsal nucleus of the thalamus. Annals of Neurology 17:558–564CrossRefGoogle Scholar
  88. Zola-Morgan S, Squire LR, Amaral DG, Suzuki WA (1989): Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. Journal of Neuroscience 9:4355–4370Google Scholar
  89. Zola-Morgan S, Squire LR, Mishkin M (1982): The neuroanatomy of amnesia: amygdala-hippocampus versus temporal stem. Science 218:1337–1339CrossRefGoogle Scholar

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© Birkhäuser Boston 1992

Authors and Affiliations

  • Jocelyne Bachevalier
  • Mortimer Mishkin

There are no affiliations available

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