Retrograde amnesia after hippocampal damage: Recent vs. remote memories in two tasks

We review evidence from experiments conducted in our laboratory on retrograde amnesia in rats with damage to the hippocampal formation. In a new experiment reported here, we show that N‐methyl‐D‐aspartate (NMDA)‐induced hippocampal damage produced retrograde amnesia for both hidden platform and two‐choice visible platform discriminations in the Morris water task. For both problems there was a significant trend for longer training‐surgery intervals to be associated with worse retention performance. Little support is offered by our work for the concept that there is a process involving hippocampal‐dependent consolidation of memories in extrahippocampal permanent storage sites. Long‐term memory consolidation may take place within the hippocampus. The hippocampus may be involved permanently in storage and/or retrieval of a variety of relational and nonrelational memories if it was intact at the time of learning, even involving information which is definitely not affected in anterograde amnesia after hippocampal damage. Hippocampus 2001;11:27–42. © 2001 Wiley‐Liss, Inc.

[1]  L. Nadel,et al.  The medial temporal region and memory consolidation: A new hypothesis , 2014 .

[2]  J. Sweatt,et al.  Mechanisms of memory. , 2003, Journal of geriatric psychiatry and neurology.

[3]  Robert S Astur,et al.  Retrograde amnesia and selective damage to the hippocampal formation: memory for places and object discriminations , 1999, Behavioural Brain Research.

[4]  R. Sutherland,et al.  Hippocampal lesions produce a temporally graded retrograde amnesia on a dry version of the Morris swimming task , 1999, Psychobiology.

[5]  L. Nadel,et al.  Memory consolidation, retrograde amnesia and the hippocampal complex , 1997, Current Opinion in Neurobiology.

[6]  L. Squire,et al.  Structure and function of declarative and nondeclarative memory systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[7]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[8]  J. Hodges.  Memory, Amnesia and the Hippocampal System , 1995 .

[9]  Joseph E LeDoux,et al.  Lesions of the dorsal hippocampal formation interfere with background but not foreground contextual fear conditioning. , 1994, Learning & memory.

[10]  J. Bolhuis,et al.  Retrograde Amnesia and Memory Reactivation in Rats with Ibotenate Lesions to the Hippocampus or Subiculum , 1994, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[11]  N. Hunkin,et al.  Bilateral temporal lobe pathology with sparing of medial temporal lobe structures: Lesion profile and pattern of memory disorder , 1994, Neuropsychologia.

[12]  M. Fanselow,et al.  Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. , 1993, Behavioral neuroscience.

[13]  L. Jarrard,et al.  Selective excitotoxic pathology in the rat hippocampus , 1993, Neuropathology and applied neurobiology.

[14]  D. Gaffan,et al.  Additive effects of forgetting and fornix transection in the temporal gradient of retrograde amnesia , 1993, Neuropsychologia.

[15]  H. Markowitsch,et al.  Retrograde amnesia after traumatic injury of the fronto-temporal cortex. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[16]  T. Durkin,et al.  Time gradient for post-test vulnerability to scopolamine-induced amnesia following the initial acquisition session of a spatial reference memory task in mice. , 1993, Behavioral and neural biology.

[17]  E. Renzi,et al.  Dense Retrograde Amnesia, Intact Learning Capability and Abnormal Forgetting Rate: A Consolidation Deficit? , 1993, Cortex.

[18]  D. Béracochéa,et al.  Extended temporal gradient for the retrograde and anterograde amnesia produced by ibotenate entorhinal cortex lesions in mice , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[20]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[21]  J. W. Rudy,et al.  Some properties of configural learning: an investigation of the transverse-patterning problem. , 1992, Journal of experimental psychology. Animal behavior processes.

[22]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[23]  E. Wood,et al.  Object-recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala , 1992, Psychobiology.

[24]  E. H. Burrows,et al.  Focal retrograde amnesia following bilateral temporal lobe pathology. A neuropsychological and magnetic resonance study. , 1992, Brain : a journal of neurology.

[25]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[26]  R. C. Honey,et al.  Conditioning and contextual retrieval in hippocampal rats. , 1991, Behavioral neuroscience.

[27]  W. Barr,et al.  Retrograde amnesia following unilateral temporal lobectomy , 1990, Neuropsychologia.

[28]  R. Morris,et al.  Ibotenate Lesions of Hippocampus and/or Subiculum: Dissociating Components of Allocentric Spatial Learning , 1990, The European journal of neuroscience.

[29]  L. Squire,et al.  The primate hippocampal formation: evidence for a time-limited role in memory storage. , 1990, Science.

[30]  G. Winocur.  Anterograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions , 1990, Behavioural Brain Research.

[31]  R. J. McDonald,et al.  Hippocampus, amygdala, and memory deficits in rats , 1990, Behavioural Brain Research.

[32]  P. Milner.  A cell assembly theory of hippocampal amnesia , 1989, Neuropsychologia.

[33]  L. Squire,et al.  Autobiographical memory and amnesia , 1989 .

[34]  R. Sutherland,et al.  The hippocampal formation is necessary for rats to learn and remember configural discriminations , 1989, Behavioural Brain Research.

[35]  R. Sutherland,et al.  Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia , 1989, Psychobiology.

[36]  Arthur P. Shimamura,et al.  The neurology of memory: quantitative assessment of retrograde amnesia in two groups of amnesic patients , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  E. Granholm,et al.  Retrograde amnesia in patients with Alzheimer's disease or Huntington's disease , 1988, Neurobiology of Aging.

[38]  D. Stuss,et al.  The neuropsychology of paramedian thalamic infarction , 1988, Brain and Cognition.

[39]  Daniel L. Schacter,et al.  Priming of semantic autobiographical knowledge: A case study of retrograde amnesia , 1988, Brain and Cognition.

[40]  Rosaleen A. McCarthy,et al.  The fractionation of retrograde amnesia , 1988, Brain and Cognition.

[41]  H J Sagar,et al.  Remote memory function in Alzheimer's disease and Parkinson's disease. , 1988, Brain : a journal of neurology.

[42]  J J Miller,et al.  Long-term increases in dentate granule cell responsivity accompany operant conditioning , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  D. Salmon,et al.  Remote memory in a patient with amnesia due to hypoxia , 1987, Psychological Medicine.

[44]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  David P. Salmon,et al.  Retrograde amnesia following combined hippocampus-amygdala lesions in monkeys , 1987, Psychobiology.

[46]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  J. N. P. Rawlins,et al.  The effects of hippocampal lesions upon spatial and non-spatial tests of working memory , 1986, Behavioural Brain Research.

[48]  P. Gage.  Performance of hippocampectomized rats in a reference/working-memory task: Effects of preoperative versus postoperative training , 1985 .

[49]  E. Halgren,et al.  Recall deficits produced by afterdischarges in the human hippocampal formation and amygdala. , 1985, Electroencephalography and clinical neurophysiology.

[50]  J. Rawlins,et al.  Associations across time: The hippocampus as a temporary memory store , 1985, Behavioral and Brain Sciences.

[51]  A R Damasio,et al.  Amnesia following basal forebrain lesions. , 1985, Archives of neurology.

[52]  L. Squire,et al.  Preserved memory in retrograde amnesia: Sparing of a recently acquired skill , 1984, Neuropsychologia.

[53]  M. Rousseaux,et al.  Amnesie Retrograde Post Traumatique , 1984, Cortex.

[54]  S. Corkin.  Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

[55]  L. Cermak,et al.  The anterograde and retrograde retrieval ability of a patient with amnesia due to encephalitis , 1983, Neuropsychologia.

[56]  R. F. Thompson,et al.  Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. , 1983, Journal of neurophysiology.

[57]  R. Sutherland,et al.  A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat , 1983, Behavioural Brain Research.

[58]  C. Poser,et al.  Retrograde Amnesia For Forty Years , 1982, Cortex.

[59]  Bryan Kolb,et al.  Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat , 1982, Neuroscience Letters.

[60]  M. Mishkin.  A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[61]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[62]  M. Albert,et al.  Patterns of remote memory in amnesic and demented patients. , 1981, Archives of neurology.

[63]  S. Sara.  Memory deficits in rats with hippocampal or cortical lesions: retrograde effects. , 1981, Behavioral and neural biology.

[64]  Alfred W. Kaszniak,et al.  Remote Memory in Senile Dementia , 1981, Cortex.

[65]  Richard Hirsh,et al.  The hippocampus, conditional operations, and cognition , 1980 .

[66]  L. Nadel,et al.  Context and conditioning: A place for space , 1980 .

[67]  M. Eckardt.  The Hippocampus as a Cognitive Map , 1980 .

[68]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

[69]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[70]  M. Mishkin.  Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[71]  C. Whitty.  Amnesia. Clinical, Psychological and Medicolegal Aspects , 1978 .

[72]  D. Olton,et al.  Remembrance of places passed: Spatial memory in rats. , 1976 .

[73]  L R Squire,et al.  Retrograde amnesia: temporal gradient in very long term memory following electroconvulsive therapy. , 1975, Science.

[74]  R. Hirsh.  The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

[75]  N. Spear.  Retrieval of memory in animals. , 1973 .

[76]  D Marr,et al.  Simple memory: a theory for archicortex. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[77]  S. Ochs.  Integrative Activity of the Brain: An Interdisciplinary Approach , 1968 .

[78]  L. B. Flexner,et al.  Memory in Mice Analyzed with Antibiotics , 1967, Science.

[79]  F. Rose,et al.  Persistent memory defect following encephalitis. , 1960, Brain : a journal of neurology.

[80]  B. Milner.  The memory defect in bilateral hippocampal lesions. , 1959, Psychiatric research reports.

[81]  W. Penfield,et al.  Memory deficit produced by bilateral lesions in the hippocampal zone. , 1958, A.M.A. archives of neurology and psychiatry.

[82]  A. Walker.  Recent memory impairment in unilateral temporal lesions. , 1957, A.M.A. archives of neurology and psychiatry.

[83]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[84]  J. Zubin,et al.  Effect of Electric Convulsive Therapy on Memory , 1941 .

[85]  L. T. Robertson.  Memory and the brain. , 2002, Journal of dental education.

[86]  R. Sutherland,et al.  Configural association theory and the hippocampal formation: An appraisal and reconfiguration , 1995, Hippocampus.

[87]  L. Squire,et al.  The structure and organization of memory. , 1993, Annual review of psychology.

[88]  R. J. McDonald,et al.  A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. , 1993, Behavioral neuroscience.

[89]  H. Eichenbaum,et al.  The hippocampus--what does it do? , 1992, Behavioral and neural biology.

[90]  P. Holland,et al.  Preserved configural learning and spatial learning impairment in rats with hippocampal damage , 1992, Hippocampus.

[91]  A. Yamadori,et al.  Isolated prolonged retrograde amnesia. , 1992, European neurology.

[92]  L. Jarrard,et al.  On the hippocampus and learned conditional responding: Effects of aspiration versus ibotenate lesions , 1991, Hippocampus.

[93]  G. V. Van Hoesen,et al.  Diencephalic amnesia. , 1990, Brain : a journal of neurology.

[94]  M. Arbib.  Brains, Machines, and Mathematics , 1987, Springer US.

[95]  E. Tulving.  Multiple memory systems and consciousness. , 1987, Human neurobiology.

[96]  P. Balsam,et al.  Context and Learning , 1985 .

[97]  W. B. Orr,et al.  Hippocampectomy disrupts acquisition and retention of learned conditional responding. , 1984, Behavioral neuroscience.

[98]  Herbert Weingartner,et al.  Memory consolidation : psychobiology of cognition , 1984 .

[99]  L. Squire,et al.  Retrograde amnesia and bilateral electroconvulsive therapy. Long-term follow-up. , 1981, Archives of general psychiatry.

[100]  W A Wickelgren,et al.  Chunking and consolidation: a theoretical synthesis of semantic networks, configuring in conditioning, S--R versus congenitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system. , 1979, Psychological review.

[101]  D. Medin.  A theory of context in discrimination learning , 1975 .

[102]  W. Estes.  Memory and conditioning. , 1973 .

[103]  F. J. McGuigan,et al.  Contemporary approaches to conditioning and learning , 1973 .

[104]  B. Milner,et al.  Disorders of learning and memory after temporal lobe lesions in man. , 1972, Clinical neurosurgery.

[105]  E K Warrington,et al.  Memory for remote events in amnesic patients. , 1971, Brain : a journal of neurology.

[106]  S. Sharpless,et al.  Retrograde amnesia produced by anesthetic and convulsant agents. , 1961, Journal of comparative and physiological psychology.

[107]  W. Penfield,et al.  The effect of hippocampal lesions on recent memory. , 1955, Transactions of the American Neurological Association.

[108]  W. Russell,et al.  Traumatic amnesia. , 1946, Brain : a journal of neurology.

[109]  T. Ribot,et al.  The Diseases of Memory , 1906 .

[110]  Robert Morris Ogden,et al.  Retroactive Amnesia: Illustrative Cases and Tentative Explanation. , 1904 .

[111]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.