Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1997 Oct 29;352(1360):1461–1467. doi: 10.1098/rstb.1997.0132

Hierarchical organization of cognitive memory.

M Mishkin 1, W A Suzuki 1, D G Gadian 1, F Vargha-Khadem 1
PMCID: PMC1692056  PMID: 9368934

Abstract

This paper addresses the question of the organization of memory processes within the medial temporal lobe. Evidence obtained in patients with late-onset amnesia resulting from medial temporal pathology has given rise to two opposing interpretations of the effects of such damage on long-term cognitive memory. One view is that cognitive memory, including memory for both facts and events, is served in a unitary manner by the hippocampus and its surrounding cortices; the other is that the basic function affected in amnesia is event memory, the memory for factual material often showing substantial preservation. Recent findings in patients with amnesia resulting from relatively selective hippocampal damage sustained early in life suggest a possible reconciliation of the two views. The new findings suggest that the hippocampus may be especially important for event as opposed to fact memory, with the surrounding cortical areas contributing to both. Evidence from neuroanatomical and neurobehavioural studies in monkeys is presented in support of this proposal.

Full Text

The Full Text of this article is available as a PDF (126.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Angeli S. J., Murray E. A., Mishkin M. Hippocampectomized monkeys can remember one place but not two. Neuropsychologia. 1993 Oct;31(10):1021–1030. doi: 10.1016/0028-3932(93)90030-4. [DOI] [PubMed] [Google Scholar]
  2. Corkin S., Amaral D. G., González R. G., Johnson K. A., Hyman B. T. H. M.'s medial temporal lobe lesion: findings from magnetic resonance imaging. J Neurosci. 1997 May 15;17(10):3964–3979. doi: 10.1523/JNEUROSCI.17-10-03964.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Gabrieli J. D., Cohen N. J., Corkin S. The impaired learning of semantic knowledge following bilateral medial temporal-lobe resection. Brain Cogn. 1988 Apr;7(2):157–177. doi: 10.1016/0278-2626(88)90027-9. [DOI] [PubMed] [Google Scholar]
  4. Gadian D. G., Isaacs E. B., Cross J. H., Connelly A., Jackson G. D., King M. D., Neville B. G., Vargha-Khadem F. Lateralization of brain function in childhood revealed by magnetic resonance spectroscopy. Neurology. 1996 Apr;46(4):974–977. doi: 10.1212/wnl.46.4.974. [DOI] [PubMed] [Google Scholar]
  5. Glisky E. L., Schacter D. L., Tulving E. Computer learning by memory-impaired patients: acquisition and retention of complex knowledge. Neuropsychologia. 1986;24(3):313–328. doi: 10.1016/0028-3932(86)90017-5. [DOI] [PubMed] [Google Scholar]
  6. Hamann S. B., Squire L. R. On the acquisition of new declarative knowledge in amnesia. Behav Neurosci. 1995 Dec;109(6):1027–1044. doi: 10.1037//0735-7044.109.6.1027. [DOI] [PubMed] [Google Scholar]
  7. Horner M. D. Psychobiological evidence for the distinction between episodic and semantic memory. Neuropsychol Rev. 1990 Dec;1(4):281–321. doi: 10.1007/BF01109027. [DOI] [PubMed] [Google Scholar]
  8. Insausti R., Amaral D. G., Cowan W. M. The entorhinal cortex of the monkey: II. Cortical afferents. J Comp Neurol. 1987 Oct 15;264(3):356–395. doi: 10.1002/cne.902640306. [DOI] [PubMed] [Google Scholar]
  9. Jackson G. D., Connelly A., Duncan J. S., Grünewald R. A., Gadian D. G. Detection of hippocampal pathology in intractable partial epilepsy: increased sensitivity with quantitative magnetic resonance T2 relaxometry. Neurology. 1993 Sep;43(9):1793–1799. doi: 10.1212/wnl.43.9.1793. [DOI] [PubMed] [Google Scholar]
  10. Jones E. G., Powell T. P. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain. 1970;93(4):793–820. doi: 10.1093/brain/93.4.793. [DOI] [PubMed] [Google Scholar]
  11. Martin-Elkins C. L., Horel J. A. Cortical afferents to behaviorally defined regions of the inferior temporal and parahippocampal gyri as demonstrated by WGA-HRP. J Comp Neurol. 1992 Jul 8;321(2):177–192. doi: 10.1002/cne.903210202. [DOI] [PubMed] [Google Scholar]
  12. McKoon G., Ratcliff R., Dell G. S. A critical evaluation of the semantic-episodic distinction. J Exp Psychol Learn Mem Cogn. 1986 Apr;12(2):295–306. doi: 10.1037//0278-7393.12.2.295. [DOI] [PubMed] [Google Scholar]
  13. Meunier M., Bachevalier J., Mishkin M., Murray E. A. Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. J Neurosci. 1993 Dec;13(12):5418–5432. doi: 10.1523/JNEUROSCI.13-12-05418.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Murray E. A., Gaffan D., Mishkin M. Neural substrates of visual stimulus-stimulus association in rhesus monkeys. J Neurosci. 1993 Oct;13(10):4549–4561. doi: 10.1523/JNEUROSCI.13-10-04549.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Murray E. A., Mishkin M. Amygdalectomy impairs crossmodal association in monkeys. Science. 1985 May 3;228(4699):604–606. doi: 10.1126/science.3983648. [DOI] [PubMed] [Google Scholar]
  16. Murray E. A., Mishkin M. Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. J Neurosci. 1986 Jul;6(7):1991–2003. doi: 10.1523/JNEUROSCI.06-07-01991.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ostergaard A., Squire L. R. Childhood amnesia and distinctions between forms of memory: a comment on Wood, Brown, and Felton. Brain Cogn. 1990 Nov;14(2):127–133. doi: 10.1016/0278-2626(90)90024-i. [DOI] [PubMed] [Google Scholar]
  18. Parkinson J. K., Murray E. A., Mishkin M. A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci. 1988 Nov;8(11):4159–4167. doi: 10.1523/JNEUROSCI.08-11-04159.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rempel-Clower N. L., Zola S. M., Squire L. R., Amaral D. G. Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation. J Neurosci. 1996 Aug 15;16(16):5233–5255. doi: 10.1523/JNEUROSCI.16-16-05233.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. SCOVILLE W. B., MILNER B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry. 1957 Feb;20(1):11–21. doi: 10.1136/jnnp.20.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Shimamura A. P., Squire L. R. Impaired priming of new associations in amnesia. J Exp Psychol Learn Mem Cogn. 1989 Jul;15(4):721–728. doi: 10.1037//0278-7393.15.4.721. [DOI] [PubMed] [Google Scholar]
  22. Spiegler B. J., Mishkin M. Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations. Behav Brain Res. 1981 Nov;3(3):303–317. doi: 10.1016/0166-4328(81)90002-4. [DOI] [PubMed] [Google Scholar]
  23. Squire L. R. The neuropsychology of human memory. Annu Rev Neurosci. 1982;5:241–273. doi: 10.1146/annurev.ne.05.030182.001325. [DOI] [PubMed] [Google Scholar]
  24. Squire L. R., Zola S. M. Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13515–13522. doi: 10.1073/pnas.93.24.13515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Suzuki W. A., Amaral D. G. Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J Comp Neurol. 1994 Dec 22;350(4):497–533. doi: 10.1002/cne.903500402. [DOI] [PubMed] [Google Scholar]
  26. Suzuki W. A., Amaral D. G. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. J Neurosci. 1994 Mar;14(3 Pt 2):1856–1877. doi: 10.1523/JNEUROSCI.14-03-01856.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Suzuki W. A., Zola-Morgan S., Squire L. R., Amaral D. G. Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci. 1993 Jun;13(6):2430–2451. doi: 10.1523/JNEUROSCI.13-06-02430.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Van Hoesen G., Pandya D. N., Butters N. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents. Brain Res. 1975 Sep 12;95(1):25–38. doi: 10.1016/0006-8993(75)90205-x. [DOI] [PubMed] [Google Scholar]
  29. Van Hoesen G., Pandya D. N. Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res. 1975 Sep 12;95(1):1–24. doi: 10.1016/0006-8993(75)90204-8. [DOI] [PubMed] [Google Scholar]
  30. Van Paesschen W., Connelly A., King M. D., Jackson G. D., Duncan J. S. The spectrum of hippocampal sclerosis: a quantitative magnetic resonance imaging study. Ann Neurol. 1997 Jan;41(1):41–51. doi: 10.1002/ana.410410109. [DOI] [PubMed] [Google Scholar]
  31. Vargha-Khadem F., Gadian D. G., Watkins K. E., Connelly A., Van Paesschen W., Mishkin M. Differential effects of early hippocampal pathology on episodic and semantic memory. Science. 1997 Jul 18;277(5324):376–380. doi: 10.1126/science.277.5324.376. [DOI] [PubMed] [Google Scholar]
  32. Wood F. B., Brown I. S., Felton R. H. Long-term follow-up of a childhood amnesic syndrome. Brain Cogn. 1989 May;10(1):76–86. doi: 10.1016/0278-2626(89)90076-6. [DOI] [PubMed] [Google Scholar]
  33. Zola-Morgan S., Squire L. R., Amaral D. G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci. 1986 Oct;6(10):2950–2967. doi: 10.1523/JNEUROSCI.06-10-02950.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zola-Morgan S., Squire L. R., Amaral D. G., Suzuki W. A. Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J Neurosci. 1989 Dec;9(12):4355–4370. doi: 10.1523/JNEUROSCI.09-12-04355.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zola-Morgan S., Squire L. R., Clower R. P., Rempel N. L. Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation. J Neurosci. 1993 Jan;13(1):251–265. doi: 10.1523/JNEUROSCI.13-01-00251.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zola-Morgan S., Squire L. R., Ramus S. J. Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system. Hippocampus. 1994 Aug;4(4):483–495. doi: 10.1002/hipo.450040410. [DOI] [PubMed] [Google Scholar]
  37. Zola-Morgan S., Squire L. R., Rempel N. L., Clower R. P., Amaral D. G. Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci. 1992 Jul;12(7):2582–2596. doi: 10.1523/JNEUROSCI.12-07-02582.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES