Home LiteratureArticle Details
PMID: 8756452 Published · ppublish English Case Reports Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Three cases of enduring memory impairment after bilateral damage limited to the hippocampal formation.

Rempel-Clower NL, Zola SM, Squire LR, Amaral DG

Abstract

Patient RB (Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus, S. Zola-Morgan, L. R. Squire, and D. G. Amaral, 1986, J Neurosci 6:2950-2967) was the first reported case of human amnesia in which detailed neuropsychological analyses and detailed postmortem neuropathological analyses demonstrated that damage limited to the hippocampal formation was sufficient to produce anterograde memory impairment. Neuropsychological and postmortem neuropathological findings are described here for three additional amnesic patients with bilateral damage limited to the hippocampal formation. Findings from these patients, taken together with the findings from patient RB and other amnesic patients, make three important points about memory. (1) Bilateral damage limited primarily to the CA1 region of the hippocampal formation is sufficient to produce moderately severe anterograde memory impairment. (2) Bilateral damage beyond, the CA1 region, but still limited to the hippocampal formation, can produce more severe anterograde memory impairment. (3) Extensive, temporally graded retrograde amnesia covering 15 years or more can occur after damage limited to the hippocampal formation. Findings from studies with experimental animals are consistent with the findings from amnesic patients. The present results substantiate the idea that severity of memory impairment is dependent on locus and extent of damage within the hippocampal formation and that damage to the hippocampal formation can cause temporally graded retrograde amnesia.

MeSH Terms
Aged Amnesia/etiology,psychology Brain/pathology Brain Injuries/complications,pathology Cognition Diencephalon/pathology Fatal Outcome Hippocampus/injuries,pathology Humans Male Memory Middle Aged Neuropsychological Tests Temporal Lobe/pathology
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Rempel-Clower N L
Veterans Affairs Medical Center, San Diego, California 92161, USA.
Zola S M
Squire L R
Amaral D G
References (72)
72 references, click to expand
  1. 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):483-95 PMID: 7874239
  2. Diencephalic amnesia: a reorientation towards tracts?
    Brain Res. 1988 Dec;472(4):351-70 PMID: 3066440
  3. Amnesia with hippocampal lesions after cardiopulmonary arrest.
    Neurology. 1984 May;34(5):679-81 PMID: 6538660
  4. Are hippocampal lesions sufficient to cause lasting amnesia?
    J Neurol Neurosurg Psychiatry. 1982 Mar;45(3):243-7 PMID: 7086444
  5. Role of the hippocampal formation in learning and memory.
    Hippocampus. 1993;3 Spec No:203-17 PMID: 8287098
  6. On the course of forgetting in very long-term memory.
    J Exp Psychol Learn Mem Cogn. 1989 Mar;15(2):241-5 PMID: 2522513
  7. Retrograde amnesia and memory consolidation: a neurobiological perspective.
    Curr Opin Neurobiol. 1995 Apr;5(2):169-77 PMID: 7620304
  8. The neurology of memory: quantitative assessment of retrograde amnesia in two groups of amnesic patients.
    J Neurosci. 1989 Mar;9(3):828-39 PMID: 2926483
  9. Mnemonic and neuropathological effects of occluding the posterior cerebral artery in Macaca mulatta.
    Neuropsychologia. 1989;27(1):83-105 PMID: 2710318
  10. Remote memory as affected by aging.
    Neuropsychologia. 1974 Oct;12(4):429-35 PMID: 4437741
  11. The primate hippocampal formation: evidence for a time-limited role in memory storage.
    Science. 1990 Oct 12;250(4978):288-90 PMID: 2218534
  12. Amnesia due to Lesions Confined to the Hippocampus: A Clinical-Pathologic Study.
    J Cogn Neurosci. 1990 Summer;2(3):246-57 PMID: 23972048
  13. What causes infarction in ischemic brain?: The Robert Wartenberg Lecture.
    Neurology. 1983 Feb;33(2):222-33 PMID: 6681661
  14. Remote memory in a patient with amnesia due to hypoxia.
    Psychol Med. 1987 Aug;17(3):657-65 PMID: 3628626
  15. Memory and metamemory: a study of the feeling-of-knowing phenomenon in amnesic patients.
    J Exp Psychol Learn Mem Cogn. 1986 Jul;12(3):452-60 PMID: 2942629
  16. Modality-specific retrograde amnesia of fear.
    Science. 1992 May 1;256(5057):675-7 PMID: 1585183
  17. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses.
    Behav Neurosci. 1995 Apr;109(2):195-203 PMID: 7619310
  18. Bilateral destruction of the hippocampus (cornu ammonis) in a case of dementia.
    Monatsschr Psychiatr Neurol. 1952 Apr-May;123(4-5):193-204 PMID: 14947832
  19. Strength and duration of priming effects in normal subjects and amnesic patients.
    Neuropsychologia. 1987;25(1B):195-210 PMID: 3574658
  20. The mesial temporal substratum of memory. Anatomical studies in three individuals.
    Brain. 1972;95(3):599-632 PMID: 4655285
  21. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor.
    Neuroscience. 1995 Feb;64(3):665-74 PMID: 7715779
  22. Bilateral and limited amygdalohippocampal lesions causing a pure amnesic syndrome.
    Ann Neurol. 1985 Sep;18(3):314-9 PMID: 3931539
  23. Brain MR: pathologic correlation with gross and histopathology. 1. Lacunar infarction and Virchow-Robin spaces.
    AJR Am J Roentgenol. 1988 Sep;151(3):551-8 PMID: 3261517
  24. Basal forebrain infarction. A clinicopathologic correlation.
    Arch Neurol. 1987 Nov;44(11):1134-8 PMID: 3675245
  25. Amnesia after anterior communicating artery aneurysm rupture.
    Neurology. 1984 Jun;34(6):752-7 PMID: 6539437
  26. Diencephalic amnesia.
    Brain. 1990 Feb;113 ( Pt 1):1-25 PMID: 2302527
  27. A rapid myelin stain for frozen sections: modification of the Heidenhain procedure.
    J Neurosci Methods. 1983 Mar;7(3):289-94 PMID: 6188930
  28. Neuroanatomy of memory.
    Annu Rev Neurosci. 1993;16:547-63 PMID: 8460903
  29. A re-appraisal of a case of persistent global amnesia following right temporal lobectomy: a clinico-pathological study.
    Neuropsychologia. 1992 May;30(5):437-50 PMID: 1620324
  30. Intact text-specific reading skill in amnesia.
    J Exp Psychol Learn Mem Cogn. 1990 Nov;16(6):1068-76 PMID: 2148580
  31. Intracranial metastases in small cell carcinoma of the lung: correlation of clinical and autopsy findings.
    Cancer. 1982 Dec 1;50(11):2433-7 PMID: 6182974
  32. Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys.
    J Neurosci. 1995 May;15(5 Pt 2):3796-807 PMID: 7751947
  33. Preserved learning and memory in amnesia: intact adaptation-level effects and learning of stereoscopic depth.
    Behav Neurosci. 1989 Jun;103(3):538-47 PMID: 2736068
  34. [Memory loss with lesions of hippocampal formation. Report of a case with some remarks on the anatomical basis of memory].
    Arch Neurol. 1961 Sep;5:244-63 PMID: 13781172
  35. Distribution of brain metastases.
    Arch Neurol. 1988 Jul;45(7):741-4 PMID: 3390029
  36. Ischemic brain damage and memory impairment: a commentary.
    Hippocampus. 1996;6(5):546-52 PMID: 8953307
  37. Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy.
    J Neurosci. 1990 Jan;10(1):267-82 PMID: 1688934
  38. Impaired priming of new associations in amnesia.
    J Exp Psychol Learn Mem Cogn. 1989 Jul;15(4):721-8 PMID: 2526859
  39. Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia.
    J Neurosci. 1990 Sep;10(9):3106-17 PMID: 2118948
  40. About the clinical picture after circumscribed failure of the ammonium cortex on both sides; a contribution to the knowledge of the function of the ammon horn.
    Monatsschr Psychiatr Neurol. 1947;113(1):1-16 PMID: 20297195
  41. Normal acquisition of novel verbal information in amnesia.
    J Exp Psychol Learn Mem Cogn. 1991 Nov;17(6):1095-104 PMID: 1838384
  42. Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions.
    Behav Brain Res. 1990 May 7;38(2):145-54 PMID: 2363834
  43. Cerebral ischemia: are the memory deficits associated with hippocampal cell loss?
    Hippocampus. 1996;6(5):553-60 PMID: 8953308
  44. Memory deficit produced by bilateral lesions in the hippocampal zone.
    AMA Arch Neurol Psychiatry. 1958 May;79(5):475-97 PMID: 13519951
  45. 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):2950-67 PMID: 3760943
  46. Memory for remote events in anterograde amnesia: recognition of public figures from newsphotographs.
    Neuropsychologia. 1975 Sep;13(3):353-64 PMID: 1161134
  47. The entorhinal cortex of the monkey: II. Cortical afferents.
    J Comp Neurol. 1987 Oct 15;264(3):356-95 PMID: 2445796
  48. The information acquired during artificial grammar learning.
    J Exp Psychol Learn Mem Cogn. 1994 Jan;20(1):79-91 PMID: 8138790
  49. Retrograde amnesia: temporal gradient in very long term memory following electroconvulsive therapy.
    Science. 1975 Jan 10;187(4171):77-9 PMID: 1109228
  50. Autobiographical memory in the aged.
    Can J Psychol. 1979 Jun;33(2):118-24 PMID: 487289
  51. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans.
    Psychol Rev. 1992 Apr;99(2):195-231 PMID: 1594723
  52. P300 from amnesic patients with bilateral hippocampal lesions.
    Electroencephalogr Clin Neurophysiol. 1993 Jun;86(6):408-17 PMID: 7686475
  53. Enduring memory impairment in monkeys after ischemic damage to the hippocampus.
    J Neurosci. 1992 Jul;12(7):2582-96 PMID: 1613549
  54. Extended temporal gradient for the retrograde and anterograde amnesia produced by ibotenate entorhinal cortex lesions in mice.
    J Neurosci. 1993 Apr;13(4):1759-66 PMID: 8463849
  55. Loss of recent memory after bilateral hippocampal lesions.
    J Neurol Neurosurg Psychiatry. 1957 Feb;20(1):11-21 PMID: 13406589
  56. Cognitive impairment following frontal lobe damage and its relevance to human amnesia.
    Behav Neurosci. 1989 Jun;103(3):548-60 PMID: 2736069
  57. Remote memory in a patient with circumscribed amnesia.
    Brain Cogn. 1988 Apr;7(2):201-11 PMID: 3377899
  58. On the role of the hippocampus in learning and memory in the rat.
    Behav Neural Biol. 1993 Jul;60(1):9-26 PMID: 8216164
  59. Memory. Autopsy findings and comments on the role of hippocampus in experiential recall.
    Arch Neurol. 1974 Sep;31(3):145-54 PMID: 4853159
  60. Observations on the brains of demented old people.
    J Neurol Sci. 1970 Sep;11(3):205-42 PMID: 5505685
  61. Procedural learning in a patient with amnesia due to hypoxia.
    Brain Cogn. 1987 Oct;6(4):386-402 PMID: 3117075
  62. Memory consolidation and the medial temporal lobe: a simple network model.
    Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7041-5 PMID: 8041742
  63. Probabilistic classification learning in amnesia.
    Learn Mem. 1994 Jul-Aug;1(2):106-20 PMID: 10467589
  64. The human entorhinal cortex: a cytoarchitectonic analysis.
    J Comp Neurol. 1995 May 1;355(2):171-98 PMID: 7541808
  65. "Pure" memory loss with hippocampal lesions: a case report.
    Trans Am Neurol Assoc. 1968;93:31-4 PMID: 5711048
  66. Observations on the brains of non-demented old people.
    J Neurol Sci. 1968 Sep-Oct;7(2):331-56 PMID: 5707082
  67. Nonverbal priming in amnesia.
    Mem Cognit. 1992 Jul;20(4):441-8 PMID: 1495406
  68. Amnesia following basal forebrain lesions.
    Arch Neurol. 1985 Mar;42(3):263-71 PMID: 3977657
  69. Amnesia following a discrete basal forebrain lesion.
    Brain. 1992 Dec;115 ( Pt 6):1827-47 PMID: 1486463
  70. Pure memory loss with hippocampal lesions: a pneumoencephalographic study.
    Arch Neurol. 1979 Jan;36(1):54-6 PMID: 420610
  71. Comparative incidence of cerebrovascular lesions in normotensive and hypertensive patients.
    Neurology. 1968 Mar;18(3):255-9 PMID: 5689666
  72. Intact and long-lasting repetition priming in amnesia.
    J Exp Psychol Learn Mem Cogn. 1992 May;18(3):509-20 PMID: 1534352
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1996-08-15
Pages
5233-55
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6579309
Subset
IM
Grants
NIMH NIH HHS · R01 MH024600 · United States
NINDS NIH HHS · R01 NS016980 · United States
NIMH NIH HHS · R37 MH024600 · United States
NIMH NIH HHS · MH24600 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]