Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus

Zola-Morgan, S; Squire, LR; Amaral, DG

doi:10.1523/jneurosci.06-10-02950.1986

Cited by 1,997Memory and Neural MechanismsMemory Processes and InfluencesCognitive Functions and Memory

Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus

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Zola-Morgan, S, Squire, LR, Amaral, DG·1986·The Journal of Neuroscience

DOI 10.1523/jneurosci.06-10-02950.1986PMC PMC6568782

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Abstract

During the past 100 years clinical studies of amnesia have linked memory impairment to damage of the hippocampus. Yet the damage in these cases has not usually been confined to the hippocampus, and the status of memory functions has often been based on incomplete neuropsychological information. Thus, the human cases have until now left some uncertainty as to whether lesions limited to the hippocampus are sufficient to cause amnesia. Here we report a case of amnesia in a patient (R.B.) who developed memory impairment following an ischemic episode. During the 5 years until his death, R.B. exhibited marked anterograde amnesia, little if any retrograde amnesia, and showed no signs of cognitive impairment other than memory. Thorough histological examination revealed a circumscribed bilateral lesion involving the entire CA1 field of the hippocampus. Minor pathology was found elsewhere in the brain (e.g., left globus pallidus, right postcentral gyrus, left internal capsule), but the only damage that could be reasonably associated with the memory defect was the lesion in the hippocampus. To our knowledge, this is the first reported case of amnesia following a lesion limited to the hippocampus in which extensive neuropsychological and neuropathological analyses have been carried out.

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Lesions of the hippocampus in humans and other mammals produce severe amnesia for certain memories.
“It is well known that lesions of the hippocampus in humans and other mammals produce severe amnesia for certain memories (Scoville and Milner, 1957; Morris et al., 1982; Zola-Morgan et al., 1986; reviewed by Squire, 1987).”
From The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. (1996) · cites this paper as Zola-Morgan et al., 1986

LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS
Scoville, W. B., & Milner, B. (1957) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.20.1.11 · Cited by 7,322 · see citing works
Le test de copie d'une figure complexe
Osterrieth, P. M. (1944) · Medical Entomology and Zoology · Cited by 2,337 · see citing works
Hippocampus, space, and memory
Olton, D. S., Becker, J. T., & Handelmann, G. E. (1979) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00062713 · Cited by 2,018 · see citing works
Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system.
de Nó, R. L. (1934) · Cited by 1,974 · see citing works
A new model of bilateral hemispheric ischemia in the unanesthetized rat.
Pulsinelli, W. A., & Brierley, J. B. (1979) · Stroke · doi:10.1161/01.str.10.3.267 · Cited by 1,947 · see citing works
Cell Damage in the Brain: A Speculative Synthesis
Siesjö, B. K. (1981) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1981.18 · Cited by 1,807 · see citing works
EPILEPSY AND THE TEMPORAL LOBES
Margerison, J. H., & Corsellis, J. (1966) · Brain · doi:10.1093/brain/89.3.499 · Cited by 1,260 · see citing works
The information that amnesic patients do not forget.
Graf, P., Squire, L. R., & Mandler, G. (1984) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037//0278-7393.10.1.164 · Cited by 883 · see citing works
Self-citation
Disorders of Learning and Memory after Temporal Lobe Lesions in Man
Milner, B. A. (1972) · Neurosurgery · doi:10.1093/neurosurgery/19.cn_suppl_1.421 · Cited by 882 · see citing works
THE WERNICKE-KORSAKOFF SYNDROME
Russell, R. W. R. (1972) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.35.2.277 · Cited by 815 · see citing works
Frequency of episodic memories as a function of their age
Crovitz, H. F., & Schiffman, H. (1974) · Bulletin of the Psychonomic Society · doi:10.3758/bf03334277 · Cited by 694 · see citing works
Anoxic-ischemic encephalopathy in rats.
Levine, S. (1960) · PubMed · Cited by 636 · see citing works
The parahippocampal gyrus: New observations regarding its cortical connections in the monkey
Hoesen, G. W. V. (1982) · Trends in Neurosciences · doi:10.1016/0166-2236(82)90201-6 · Cited by 624 · see citing works
Neurotoxicity of excitatory amino acids
Guidotti, A. (1990) · Raven Press eBooks · Cited by 619 · see citing works
“Epileptic” brain damage in rats induced by sustained electrical stimulation of the perforant path. I. Acute electrophysiological and light microscopic studies
Sloviter, R. S. (1983) · Brain Research Bulletin · doi:10.1016/0361-9230(83)90037-0 · Cited by 546 · see citing works
Anatomical distributions of four pharmacologically distinct 3H-L-glutamate binding sites
Monaghan, D. T., Holets, V. R., Toy, D. W., & Cotman, C. W. (1983) · Nature · doi:10.1038/306176a0 · Cited by 522 · see citing works
Amnesia Following Basal Forebrain Lesions
Damásio, A. R., Graff‐Radford, N. R., Eslinger, P. J., Damasio, H., & Kassell, N. F. (1985) · Archives of Neurology · doi:10.1001/archneur.1985.04060030081013 · Cited by 475 · see citing works
Epilepsy and Neuron Loss in the Hippocampus
Dam, A. M. (1980) · Epilepsia · doi:10.1111/j.1528-1157.1980.tb04315.x · Cited by 413 · see citing works
Priming across modalities and priming across category levels: Extending the domain of preserved function in amnesia.
Graf, P., Shimamura, A. P., & Squire, L. R. (1985) · Journal of Experimental Psychology Learning Memory and Cognition · doi:10.1037//0278-7393.11.2.386 · Cited by 410 · see citing works
Self-citation
Quantitative autoradiographic distribution of L-[3H]glutamate-binding sites in rat central nervous system
Greenamyre, J. T., Young, A., & Penney, J. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-08-02133.1984 · Cited by 351 · see citing works
Memory impairment in monkeys following lesions limited to the hippocampus.
Zola-Morgan, S. M., & Squire, L. R. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.155 · Cited by 350 · see citing works
Self-citation
Multimodal Amnesic Syndrome Following Bilateral Temporal and Basal Forebrain Damage
Damásio, A. R., Eslinger, P. J., Damasio, H., Hoesen, G. W. V., & Cornell, S. H. (1985) · Archives of Neurology · doi:10.1001/archneur.1985.04060030070012 · Cited by 310 · see citing works
Selective hippocampal lesions: Differential effects on performance by rats of a spatial task with preoperative versus postoperative training.
Jarrard, L. E. (1978) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077516 · Cited by 309 · see citing works
The Neuroanatomy of Amnesia: Amygdala-Hippocampus Versus Temporal Stem
Zola-Morgan, S. M., Squire, L. R., & Mishkin, M. (1982) · Science · doi:10.1126/science.6890713 · Cited by 308 · see citing works
Self-citation
Dorsal thalamic lesion in a noted case of human memory dysfunction
Squire, L. R., & Moore, R. Y. (1979) · Annals of Neurology · doi:10.1002/ana.410060607 · Cited by 283 · see citing works
Self-citation
Hippocampal resections impair associative learning and recognition memory in the monkey
Mahut, H., Zola-Morgan, S. M., & Moss, M. B. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-09-01214.1982 · Cited by 258 · see citing works
Self-citation
Paired-associate learning and priming effects in amnesia: A neuropsychological study.
Shimamura, A. P., & Squire, L. R. (1984) · Journal of Experimental Psychology General · doi:10.1037//0096-3445.113.4.556 · Cited by 256 · see citing works
Self-citation
Evidence for amelioration of ischaemic neuronal damage in the hippocampal formation by lesions of the perforant path
Wieloch, T. W., Lindvall, O., Blomqvist, P., & Gage, F. H. (1985) · Neurological Research · doi:10.1080/01616412.1985.11739695 · Cited by 241 · see citing works
Human memory and amnesia
Squire, L. (1984) · Neurobiology of Learning and Memory · Cited by 234 · see citing works
Self-citation
Imagery as a mnemonic aid after left temporal lobectomy: Contrast between material-specific and generalized memory disorders
Jones, M. K. (1974) · Neuropsychologia · doi:10.1016/0028-3932(74)90023-2 · Cited by 224 · see citing works
Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills
Zola-Morgan, S. M., & Squire, L. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-04-01072.1984 · Cited by 209 · see citing works
Self-citation
Behavioral performance of rats following transient forebrain ischemia.
Volpe, B. T., Pulsinelli, W. A., Tribuna, J., & Davis, H. P. (1984) · Stroke · doi:10.1161/01.str.15.3.558 · Cited by 193 · see citing works
THE NEUROLOGY OF MEMORY: THE CASE FOR CORRESPONDENCE BETWEEN THE FINDINGS FOR HUMAN AND NONHUMAN PRIMATE
Squire, L. R., & Zola-Morgan, S. M. (1983) · Elsevier eBooks · doi:10.1016/b978-0-12-213460-9.50012-5 · Cited by 183 · see citing works
Self-citation
Persistent anterograde amnesia after stab wound of the basal brain
Teuber, H., Milner, B. A., & Vaughan, H. G. (1968) · Neuropsychologia · doi:10.1016/0028-3932(68)90025-0 · Cited by 166 · see citing works
THE AMNESIC SYNDROME OF POSTERIOR CEREBRAL ARTERY OCCLUSION
Benson, D. F., Marsden, C. D., & Meadows, J. C. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1974.tb02767.x · Cited by 157 · see citing works
The amnesic syndrome: Descriptions and explanations.
Hirst, W. C. (1982) · Psychological Bulletin · doi:10.1037/0033-2909.91.3.435 · Cited by 157 · see citing works
The Characterization of an Amnesic Syndrome Following Hypoxic Ischemic Injury
Volpe, B. T., & Hirst, W. D. (1983) · Archives of Neurology · doi:10.1001/archneur.1983.04050070066017 · Cited by 148 · see citing works
l-Glutamate, excitatory amino acid receptors and brain function
Fagg, G. E. (1985) · Trends in Neurosciences · doi:10.1016/0166-2236(85)90080-3 · Cited by 134 · see citing works
Evolutionary trends in limbic structures
Stephan, H. (1983) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(83)90041-6 · Cited by 133 · see citing works
Reference and working memory of rats following hippocampal damage induced by transient forebrain ischemia
Davis, H. P., Tribuna, J., Pulsinelli, W. A., & Volpe, B. T. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90195-2 · Cited by 123 · see citing works
Excitatory amino acids and anoxic/ischaemic brain damage
Meldrum, B. S. (1985) · Trends in Neurosciences · doi:10.1016/0166-2236(85)90024-4 · Cited by 120 · see citing works
PERSISTENT MEMORY DEFECT FOLLOWING ENCEPHALITIS
Rose, F. C., & Symonds, C. P. (1960) · Brain · doi:10.1093/brain/83.2.195 · Cited by 107 · see citing works
Retention deficits after combined amygdalo-hippocampal and selective hippocampal resections in the monkey
Mahut, H., Moss, M. B., & Zola-Morgan, S. M. (1981) · Neuropsychologia · doi:10.1016/0028-3932(81)90105-6 · Cited by 107 · see citing works
Self-citation
A Preliminary Report on a New Memory Scale
Gilbert, J. G., Levee, R. F., & Catalano, F. L. (1968) · Perceptual and Motor Skills · doi:10.2466/pms.1968.27.1.277 · Cited by 100 · see citing works
Lacunes: Small, deep cerebral infarcts
Fisher, C. M. (2011) · Neurology · doi:10.1212/01.wnl.0000410087.34228.7d · Cited by 99 · see citing works
Visuoperceptive deficits in long-term alcoholics and alcoholics with Korsakoff's psychosis.
Kapur, N., & Butters, N. (1977) · Journal of Studies on Alcohol · doi:10.15288/jsa.1977.38.2025 · Cited by 98 · see citing works
The Neuropsychology of Memory: New Links between Humans and Experimental Animals
Squire, L. R., & Zola-Morgan, S. M. (1985) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1985.tb37585.x · Cited by 97 · see citing works
Self-citation
Comparative aspects of studies of amnesia
Weiskrantz, L. (1982) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1982.0075 · Cited by 97 · see citing works
A rapid myelin stain for frozen sections: modification of the Heidenhain procedure
Hutchins, B., & Weber, J. T. (1983) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(83)90012-2 · Cited by 89 · see citing works
The Medial Temporal Region and M em ory Consolidation: A New Hypothesis
Squire, L. R., Cohen, N. J., & Nadel, L. (2014) · doi:10.4324/9781315802626-13 · Cited by 89 · see citing works
Self-citation
Glutamate in hippocampal pathways.
Storm‐Mathisen, J. (1981) · PubMed · Cited by 81 · see citing works
Bilateral and limited amygdalohippocampal lesions causing a pure amnesic syndrome
Duyckaerts, C. J., Derouesné, C., Signoret, J. L., Gray, F., Escourolle, R., & Castaigne, P. (1985) · Annals of Neurology · doi:10.1002/ana.410180307 · Cited by 75 · see citing works
Human Memory and Its Pathology
Goodwin, D. W. (1971) · JAMA · doi:10.1001/jama.1971.03180170078031 · Cited by 75 · see citing works
Neuropathology of Amnesic States
Brierley, J. B. (1977) · Elsevier eBooks · doi:10.1016/b978-0-407-00056-8.50014-9 · Cited by 69 · see citing works
A Psychosocial Study of Chronic, Circumscribed Amnesia
Kaushall, P., Zetin, M., & Squire, L. R. (1981) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-198106000-00009 · Cited by 65 · see citing works
Self-citation
Amnesia: A Minimal Model and an Interpretation
Cermak, L. S. (2014) · doi:10.4324/9781315778105-23 · Cited by 65 · see citing works
Spatial features of the rat hippocampal vascular system
Coyle, P. V. (1978) · Experimental Neurology · doi:10.1016/0014-4886(78)90108-5 · Cited by 62 · see citing works
Effects of Human Hippocampal Ablation
Gol, A., & Faibish, G. M. (1967) · Journal of neurosurgery · doi:10.3171/jns.1967.26.4.0390 · Cited by 50 · see citing works
THE MESIAL TEMPORAL SUBSTRATUM OF MEMORY ANATOMICAL STUDIES IN THREE INDIVIDUALS
Buren, J. M. V., & Borke, R. C. (1972) · Brain · doi:10.1093/brain/95.3.599 · Cited by 48 · see citing works
Memory: Neural Organization and Behavior
Squire, L. R. (1987) · Comprehensive physiology · doi:10.1002/cphy.cp010508 · Cited by 43 · see citing works
Self-citation
Consolidation of memory the hippocampus revisited
Mahut, H., & Moss, M. B. (1984) · Cited by 40 · see citing works
Comparative investigations on hippocampus in insectivores and primates.
Stephan, H., & Manolescu, J. (1980) · PubMed · Cited by 33 · see citing works
Changes in local cerebral blood flow following profound systemic hypotension
Gamache, F. W., Myers, R. E., & Monell, E. (1976) · Journal of neurosurgery · doi:10.3171/jns.1976.44.2.0215 · Cited by 20 · see citing works
Amnesia with hippocampal lesions after cardiopulmonary arrest
Cummings, J. L. (1996) · Neurocase · doi:10.1093/neucas/2.4.259-g · Cited by 14 · see citing works
Neuropsychology.
Teuber, H. (1950) · Charles C Thomas Publisher eBooks · doi:10.1037/14022-003 · Cited by 13 · see citing works
"Pure" memory loss with hippocampal lesions: a case report.
DeJong, R. N., Hh, I., & Olson (1968) · PubMed · Cited by 12 · see citing works
CEREBRAL COMPLICATIONS OF HYPOTENSIVE ANAESTHESIA IN A HEALTHY ADULT
Brierley, J. B., & Cooper, J. E. (1963) · Survey of Anesthesiology · doi:10.1097/00132586-196310000-00025 · Cited by 5 · see citing works
Alterations in cerebral blood flow produced by hypotension: a comparison of methods.
Gamache, F. W., & Dold, G. (1975) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.38.8.765 · Cited by 4 · see citing works
Pure memory loss with hippocampal lesions. A pneumoencephalographic study
Muramoto, O. (1996) · Neurocase · doi:10.1093/neucas/2.4.259-x · Cited by 3 · see citing works

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Lein, E. S., Hawrylycz, M. J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A. F., Boguski, M. S., Brockway, K. S., Byrnes, E. J., et al. (2007) · Nature · doi:10.1038/nature05453 · Cited by 5,572 · see citing works
A psychobiological model of temperament and character
Cloninger, C. R. (1993) · Archives of General Psychiatry · doi:10.1001/archpsyc.1993.01820240059008 · Cited by 5,458 · see citing works
Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans.
Squire, L. R. (1992) · Psychological Review · doi:10.1037/0033-295x.99.2.195 · Cited by 5,376 · see citing works
Self-citation
Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory
McClelland, J. L., McNaughton, B. L., & O'Reilly, R. C. (1995) · Psychological Review · doi:10.1037/0033-295x.102.3.419 · Cited by 5,256 · see citing works
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Squire, L. R., & Zola-Morgan, S. (1991) · Science · doi:10.1126/science.1896849 · Cited by 3,282 · see citing works
Self-citation
The medial temporal lobe
Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144130 · Cited by 2,680 · see citing works
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The Medial Temporal Lobe and Recognition Memory
Eichenbaum, H., Yonelinas, A. P., & Ranganath, C. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094328 · Cited by 2,580 · see citing works
The human hippocampus and spatial and episodic memory
Burgess, N., Maguire, E. A., & O'Keefe, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00830-9 · Cited by 2,401 · see citing works
Dynamics of the Hippocampal Ensemble Code for Space
Wilson, M. A., & McNaughton, B. L. (1993) · Science · doi:10.1126/science.8351520 · Cited by 2,350 · see citing works
Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making
Bechara, A., Damasio, H., Damasio, A. R., & Lee, G. P. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05473.1999 · Cited by 2,001 · see citing works
Memory and the Brain
Squire, L. R. (1986) · Elsevier eBooks · doi:10.1016/b978-0-12-268330-5.50013-5 · Cited by 1,932 · see citing works
Self-citation
The Neuropsychology of Anxiety
Gray, J. A., & McNaughton, N. (2003) · doi:10.1093/acprof:oso/9780198522713.001.0001 · Cited by 1,933 · see citing works
Memory consolidation, retrograde amnesia and the hippocampal complex
Nadel, L., & Moscovitch, M. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80010-4 · Cited by 1,924 · see citing works
Episodic memory, amnesia, and the hippocampal–anterior thalamic axis
Aggleton, J. P., & Brown, M. W. (1999) · Behavioral and Brain Sciences · doi:10.1017/s0140525x99002034 · Cited by 1,879 · see citing works
Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates.
Scheltens, P., Leys, D., Barkhof, F., Huglo, D. G., Weinstein, H. C., Vermersch, P., Kuiper, M. A., Steinling, M., Wolters, E. C., & Valk, J. (1992) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.55.10.967 · Cited by 1,781 · see citing works
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · see citing works
Differential Effects of Early Hippocampal Pathology on Episodic and Semantic Memory
Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connelly, A., Van Paesschen, W., & Mishkin, M. (1997) · Science · doi:10.1126/science.277.5324.376 · Cited by 1,746 · see citing works
Functional organization of the hippocampal longitudinal axis
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3785 · Cited by 1,738 · see citing works
Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition
Damasio, A. R. (1989) · Cognition · doi:10.1016/0010-0277(89)90005-x · Cited by 1,538 · see citing works
The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition
Lupien, S. J., Maheu, F., Tu, M., Fiocco, A., & Schramek, T. E. (2007) · Brain and Cognition · doi:10.1016/j.bandc.2007.02.007 · Cited by 1,474 · see citing works
Retrograde amnesia and memory consolidation: a neurobiological perspective
Squire, L. R., & Alvarez, P. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80023-9 · Cited by 1,412 · see citing works
Self-citation
Patients with hippocampal amnesia cannot imagine new experiences
Hassabis, D., Kumaran, D., Vann, S. D., & Maguire, E. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610561104 · Cited by 1,414 · see citing works
Double Dissociation of Conditioning and Declarative Knowledge Relative to the Amygdala and Hippocampus in Humans
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A. R. (1995) · Science · doi:10.1126/science.7652558 · Cited by 1,400 · see citing works
Structure and function of declarative and nondeclarative memory systems
Squire, L. R., & Zola, S. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13515 · Cited by 1,327 · see citing works
Self-citation
Functional Heterogeneity in Cingulate Cortex: The Anterior Executive and Posterior Evaluative Regions
Vogt, B. A., Finch, D. M., & Olson, C. R. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.6.435-a · Cited by 1,315 · see citing works
The hippocampus and memory: insights from spatial processing
Bird, C. M., & Burgess, N. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2335 · Cited by 1,313 · see citing works
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,300 · see citing works
Self-citation
Memory of sequential experience in the hippocampus during slow wave sleep
Lee, A. K., & Wilson, M. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)01096-6 · Cited by 1,296 · see citing works
Mechanisms of Memory
Squire, L. R. (1986) · Science · doi:10.1126/science.3086978 · Cited by 1,278 · see citing works
Self-citation
Computational analysis of the role of the hippocampus in memory
Treves, A., & Rolls, E. T. (1994) · Hippocampus · doi:10.1002/hipo.450040319 · Cited by 1,272 · see citing works
Unbiased stereological estimation of the number of neurons in the human hippocampus
West, M. J., & Gundersen, H. J. G. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.902960102 · Cited by 1,153 · see citing works
Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents
Suzuki, W., & Amaral, D. G. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903500402 · Cited by 1,134 · see citing works
Self-citation
On the role of the hippocampus in learning and memory in the rat.
Jarrard, L. E. (1993) · Behavioral and Neural Biology · doi:10.1016/0163-1047(93)90664-4 · Cited by 1,125 · see citing works
The Structure and Organization of Memory
Squire, L. R., Knowlton, B. J., & Musen, G. (1993) · Annual Review of Psychology · doi:10.1146/annurev.ps.44.020193.002321 · Cited by 1,121 · see citing works
Self-citation
Two functional components of the hippocampal memory system
Eichenbaum, H., Otto, T., & Cohen, N. J. (1994) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00035391 · Cited by 1,094 · see citing works
Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat
Woolley, C. S., & McEwen, B. S. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903360210 · Cited by 1,073 · see citing works
Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach
Norman, K. A., & O'Reilly, R. C. (2003) · Psychological Review · doi:10.1037/0033-295x.110.4.611 · Cited by 1,312 · see citing works
The Hippocampus, Memory, and Place Cells
Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M., & Tanila, H. (1999) · Neuron · doi:10.1016/s0896-6273(00)80773-4 · Cited by 1,064 · see citing works
Episodic memory and beyond: the hippocampus and neocortex in transformation
Moscovitch, M., Cabeza, R., Winocur, G., & Nadel, L. (2016) · Annual Review of Psychology · doi:10.1146/annurev-psych-113011-143733 · Cited by 1,062 · see citing works
Autophosphorylation at Thr <sup>286</sup> of the α Calcium-Calmodulin Kinase II in LTP and Learning
Giese, K. P., Fedorov, N. B., Filipkowski, R. K., & Silva, A. J. (1998) · Science · doi:10.1126/science.279.5352.870 · Cited by 1,055 · see citing works
Configural association theory: The role of the hippocampal formation in learning, memory, and amnesia
Sutherland, R. J., & Rudy, J. W. (1989) · Psychobiology · doi:10.3758/bf03337828 · Cited by 956 · see citing works
A pathophysiological framework of hippocampal dysfunction in ageing and disease
Small, S. A., Schobel, S., Buxton, R. B., Witter, M. P., & Barnes, C. A. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn3085 · Cited by 920 · see citing works
The Anatomical Connections of the Macaque Monkey Orbitofrontal Cortex. A Review
Cavada, C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.220 · Cited by 917 · see citing works
Remembering episodes: a selective role for the hippocampus during retrieval
Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y., & Engel, S. A. (2000) · Nature Neuroscience · doi:10.1038/80671 · Cited by 906 · see citing works
Selective vulnerability of the hippocampus in brain ischemia
Schmidt‐Kastner, R., & Freund, T. F. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90001-5 · Cited by 890 · see citing works
The role of the hippocampus in the pathophysiology of major depression
Campbell, S., & MacQUEEN, G. M. (2004) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0441 · Cited by 879 · see citing works
The Primate Hippocampal Formation: Evidence for a Time-Limited Role in Memory Storage
Zola-Morgan, S. M., & Squire, L. R. (1990) · Science · doi:10.1126/science.2218534 · Cited by 863 · see citing works
Self-citation
The hippocampus—what does it do?
Eichenbaum, H., Otto, T., & Cohen, N. J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90724-i · Cited by 867 · see citing works
The entorhinal cortex of the monkey: II. Cortical afferents
Insausti, R., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640306 · Cited by 835 · see citing works
Self-citation
Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation
Rempel-Clower, N., Zola, S. M., Squire, L. R., & Amaral, D. G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-16-05233.1996 · Cited by 815 · see citing works
Self-citation
Topographical disorientation: a synthesis and taxonomy
Aguirre, G. K. (1999) · Brain · doi:10.1093/brain/122.9.1613 · Cited by 772 · see citing works
The Cognitive Neuroscience of Human Memory Since H.M.
Squire, L. R., & Wixted, J. T. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113720 · Cited by 749 · see citing works
Self-citation
Neuroanatomy of Memory
Zola-Morgan, S. M., & Squire, L. R. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.16.030193.002555 · Cited by 740 · see citing works
Self-citation
Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice
Rampon, C., Tang, Y.-P., Goodhouse, J., Shimizu, E., Kyin, M., & Tsien, J. Z. (2000) · Nature Neuroscience · doi:10.1038/72945 · Cited by 737 · see citing works
Impact of aging on hippocampal function: plasticity, network dynamics, and cognition
Rosenzweig, E. S., & Barnes, C. A. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00126-0 · Cited by 730 · see citing works
Conservation of hippocampal memory function in rats and humans
Bunsey, M. D., & Eichenbaum, H. (1996) · Nature · doi:10.1038/379255a0 · Cited by 733 · see citing works
The Coupling of Neurotransmitter Receptors to Ion Channels in the Brain
Nicoll, R. A. (1988) · Science · doi:10.1126/science.2456612 · Cited by 729 · see citing works
Delayed hippocampal damage in humans following cardiorespiratory arrest
Petito, C. K., Feldmann, E. G., Pulsinelli, W. A., & Plum, F. (1987) · Neurology · doi:10.1212/wnl.37.8.1281 · Cited by 712 · see citing works
Schizophrenia, sensory gating, and nicotinic receptors
Adler, L. E., Olincy, A., Waldo, M., Harris, J. G., Griffith, J., Stevens, K., Flach, K., Nagamoto, H., Bickford, P., Leonard, S., et al. (1998) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033320 · Cited by 690 · see citing works
Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes
Pavlides, C., & Winson, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02907.1989 · Cited by 684 · see citing works
Functional anatomical studies of explicit and implicit memory retrieval tasks
Buckner, R. L., Petersen, S., Ojemann, J. G., Miezin, F. M., Squire, L., & Raichle, M. E. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00012.1995 · Cited by 678 · see citing works
Self-citation
Hippocampectomy disrupts trace eye-blink conditioning in rabbits.
Moyer, J. R., Deyo, R. A., & Disterhoft, J. F. (2015) · Behavioral Neuroscience · doi:10.1037/bne0000079 · Cited by 664 · see citing works
The Episodic Memory System: Neurocircuitry and Disorders
Dickerson, B. C., & Eichenbaum, H. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.126 · Cited by 658 · see citing works
Potential role for adult neurogenesis in the encoding of time in new memories
Aimone, J. B., Wiles, J., & Gage, F. H. (2006) · Nature Neuroscience · doi:10.1038/nn1707 · Cited by 644 · see citing works
The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging.
Stern, C. E., Corkin, S., González, R. G., Guimarães, A. R., Baker, J. R., Jennings, P. J., Carr, C. A., Sugiura, R., Vedantham, V., & Rosen, B. R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8660 · Cited by 640 · see citing works
Systemic administration of MK-801 protects against ischemia-induced hippocampal neurodegeneration in the gerbil
Gill, R., Foster, A., & Woodruff, G. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-10-03343.1987 · Cited by 640 · see citing works
Age-Related Reductions in Human Recognition Memory Due to Impaired Encoding
Grady, C. L., McIntosh, A. R., Horwitz, B., Maisog, J. M., Ungerleider, L. G., Mentis, M. J., Pietrini, P., Schapiro, M. B., & Haxby, J. V. (1995) · Science · doi:10.1126/science.7618082 · Cited by 633 · see citing works
Pain processing during three levels of noxious stimulation produces differential patterns of central activity
Derbyshire, S. W. G., Jones, A. K. P., Gyulai, F., Clark, S., Townsend, D., & Firestone, L. L. (1997) · Pain · doi:10.1016/s0304-3959(97)00138-3 · Cited by 629 · see citing works
Regionally specific loss of neurons in the aging human hippocampus.
West, M. (1993) · Neurobiology of Aging · doi:10.1016/0197-4580(93)90113-p · Cited by 638 · see citing works
The hippocampus and memory for orderly stimulus relations
Dusek, J. A., & Eichenbaum, H. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.7109 · Cited by 610 · see citing works
Impaired Hippocampal Representation of Space in CA1-Specific NMDAR1 Knockout Mice
McHugh, T. J., Blum, K. I., Tsien, J. Z., Tonegawa, S., & Wilson, M. A. (1996) · Cell · doi:10.1016/s0092-8674(00)81828-0 · Cited by 593 · see citing works
Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices
Suzuki, W., & Amaral, D. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01856.1994 · Cited by 587 · see citing works
Self-citation
Object recognition memory: Neurobiological mechanisms of encoding, consolidation and retrieval
Winters, B. D., Saksida, L. M., & Bussey, T. J. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.04.004 · Cited by 568 · see citing works
Basal cortisol levels and cognitive deficits in human aging
Lupien, S., Lecours, A., Lussier, I., Schwartz, G., Nair, N., & Meaney, M. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02893.1994 · Cited by 566 · see citing works
Hippocampal-Neocortical Interactions in Memory Formation, Consolidation, and Reconsolidation
Wang, S., & Morris, R. (2009) · Annual Review of Psychology · doi:10.1146/annurev.psych.093008.100523 · Cited by 536 · see citing works
Alzheimer Disease
Castellani, R. J., Rolston, R. K., & Smith, M. A. (2010) · Disease-a-Month · doi:10.1016/j.disamonth.2010.06.001 · Cited by 561 · see citing works
Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities
Suzuki, W., Zola-Morgan, S. M., Squire, L., & Amaral, D. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02430.1993 · Cited by 543 · see citing works
Self-citation
Place Cells, Grid Cells, and MemoryPreprint
Moser, M., Rowland, D. C., & Moser, E. I. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021808 · Cited by 538 · see citing works
NMDA Receptor-Dependent Synaptic Reinforcement as a Crucial Process for Memory Consolidation
Shimizu, E., Tang, Y., Rampon, C., & Tsien, J. Z. (2000) · Science · doi:10.1126/science.290.5494.1170 · Cited by 532 · see citing works
Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity
Yonelinas, A., Kroll, N., Quamme, J., Lazzara, M. M., Sauvé, M., Widaman, K., & Knight, R. (2002) · Nature Neuroscience · doi:10.1038/nn961 · Cited by 554 · see citing works
Ventral hippocampal lesions affect anxiety but not spatial learning
Bannerman, D. M., Grubb, M., Deacon, R. M. J., Yee, B. K., Feldon, J., & Rawlins, J. N. P. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00268-1 · Cited by 530 · see citing works
A Mitogen-Activated Protein Kinase Cascade in the CA1/CA2 Subfield of the Dorsal Hippocampus Is Essential for Long-Term Spatial Memory
Blum, S., Moore, A. N., Adams, F., & Dash, P. K. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03535.1999 · Cited by 522 · see citing works
Some Cytoarchitectural Abnormalities of the Entorhinal Cortex in Schizophrenia
Arnold, S. E. (1991) · Archives of General Psychiatry · doi:10.1001/archpsyc.1991.01810310043008 · Cited by 525 · see citing works
Alzheimer's disease: synaptic dysfunction and Aβ
Shankar, G. M., & Walsh, D. M. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-48 · Cited by 522 · see citing works
Amyloid, hypometabolism, and cognition in Alzheimer disease: An [11C]PIB and [18F]FDG PET study
Edison, P., Archer, H. A., Hinz, R., Hammers, A., Pavese, N., Tai, Y. F., Hotton, G., Cutler, D., Fox, N., Kennedy, A., et al. (2007) · Neurology · doi:10.1212/01.wnl.0000244749.20056.d4 · Cited by 518 · see citing works
Network memory
Fuster, J. M. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01128-4 · Cited by 516 · see citing works
Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex
Bohbot, V. D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., & Nadel, L. (1998) · Neuropsychologia · doi:10.1016/s0028-3932(97)00161-9 · Cited by 516 · see citing works
Hippocampal CA3 NMDA Receptors Are Crucial for Memory Acquisition of One-Time Experience
Nakazawa, K., Sun, L. D., Quirk, M. C., Rondi‐Reig, L., Wilson, M. A., & Tonegawa, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00165-x · Cited by 506 · see citing works
Delayed postischemic hypothermia: a six month survival study using behavioral and histological assessments of neuroprotection
Colbourne, F., & Corbett, D. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-11-07250.1995 · Cited by 498 · see citing works
Recognition memory and the human hippocampus.
Manns, J., Hopkins, R., Reed, J. M., Kitchener, E. G., & Squire, L. (2003) · Neuron · doi:10.1016/s0896-6273(02)01147-9 · Cited by 472 · see citing works
Self-citation
cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase
Huang, Y.-Y., Li, X.-C., & Kandel, E. R. (1994) · Cell · doi:10.1016/0092-8674(94)90401-4 · Cited by 490 · see citing works
Macaque monkey retrosplenial cortex: III. Cortical efferents
Kobayashi, Y., & Amaral, D. G. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21346 · Cited by 487 · see citing works
Self-citation
Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal–neocortical interactions
Winocur, G., Moscovitch, M., & Bontempi, B. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.04.016 · Cited by 486 · see citing works
Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data.
Yonelinas, A., Kroll, N., Dobbins, I., Lazzara, M. M., & Knight, R. (1998) · Neuropsychology · doi:10.1037/0894-4105.12.3.323 · Cited by 455 · see citing works
Neurocognitive function in obstructive sleep apnoea: A meta‐review
BUCKS, R. S., OLAITHE, M., & EASTWOOD, P. (2013) · Respirology · doi:10.1111/j.1440-1843.2012.02255.x · Cited by 483 · see citing works
Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal ltp in the range of the θ frequency
Bach, M. E., Hawkins, R. D., Osman, M., Kandel, E. R., & Mayford, M. R. (1995) · Cell · doi:10.1016/0092-8674(95)90010-1 · Cited by 475 · see citing works
Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region
Zola, S. M., Squire, L. R., Teng, E., Stefanacci, L., Buffalo, E. A., & Clark, R. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00451.2000 · Cited by 477 · see citing works
Self-citation
Entorhinal cortex pathology in Alzheimer's disease
van Hoesen, G. W., Hyman, B. T., & Damasio, A. R. (1991) · Hippocampus · doi:10.1002/hipo.450010102 · Cited by 475 · see citing works
Head direction cells and the neurophysiological basis for a sense of direction
Taube, J. S. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00004-5 · Cited by 447 · see citing works
Fear memory
Izquierdo, I., Furini, C. R. G., & Myskiw, J. C. (2016) · Physiological Reviews · doi:10.1152/physrev.00018.2015 · Cited by 453 · see citing works

Psychiatry and
Rempel-Clower, N., Zola, S. M., Squire, L. R., & Amaral, D. G. (2014)
Self-citation
Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation
Rempel-Clower, N., Zola, S. M., Squire, L. R., & Amaral, D. G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-16-05233.1996 · Cited by 815 · see citing works
Self-citation
Bilateral lesions of CA1 and CA2 fields of the hippocampus are sufficient to cause a severe amnesic syndrome in humans
Kartsounis, L. D. (1996) · Neurocase · doi:10.1093/neucas/2.4.259-s · Cited by 6 · see citing works
[Amnestic syndrome with bilateral lesions restricted to the field CA-1 of both hippocampi--a case report with CT and MRI findings].
Hirasawa, M., Nakano, M., Shiohama, N., 古宮, 泰., & Mizuno, Y. (1991) · PubMed · Cited by 1 · see citing works
Are hippocampal lesions sufficient to cause lasting amnesia?
Woods, B. T., Schoene, W. C., & Kneisley, L. (1982) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.45.3.243 · Cited by 71 · see citing works

Authors: Zola-Morgan, S., Squire, L., & Amaral, D.
Affiliations: University of California San Diego (US)
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 1986-10-01
Volume: 6
Issue: 10
Pages: 2950-2967
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.06-10-02950.1986
PMC: PMC6568782
OpenAlex: W1598800837
Cited by: 1,997
References: 69
Citations by year: 2026: 10 · 2025: 12 · 2024: 50 · 2023: 19 · 2022: 25 · 2021: 23 · 2020: 58 · 2019: 30 · 2018: 39 · 2017: 52 · 2016: 36 · 2015: 52 · 2014: 56 · 2013: 51 · 2012: 58
FWCI: 25.73
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 182 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Mental Health (MH24600)
National Institute of Neurological Disorders and Stroke (NS 20004, NS19063)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
Keywords: anterograde amnesia, hippocampal CA1, bilateral hippocampal lesions, memory impairment, ischemic stroke, medial temporal lobe, retrograde amnesia, neuropathology, neuropsychological assessment
MeSH terms: Amnesia, Cerebral Cortex, Brain Ischemia, Diencephalon, Hippocampus, Humans, Male, Memory Disorders, Middle Aged, Temporal Lobe

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Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus

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