A cortical–hippocampal system for declarative memory

Recent neurobiological studies have begun to reveal the cognitive and neural coding mechanisms that underlie declarative memory — our ability to recollect everyday events and factual knowledge. These studies indicate that the critical circuitry involves bidirectional connections between the neocortex, the parahippocampal region and the hippocampus. Each of these areas makes a unique contribution to memory processing. Widespread high-order neocortical areas provide dedicated processors for perceptual, motor or cognitive information that is influenced by other components of the system. The parahippocampal region mediates convergence of this information and extends the persistence of neocortical memory representations. The hippocampus encodes the sequences of places and events that compose episodic memories, and links them together through their common elements. Here I describe how these mechanisms work together to create and re-create fully networked representations of previous experiences and knowledge about the world.

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

[2]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[3]  D. Gaffan,et al.  Recognition impaired and association intact in the memory of monkeys after transection of the fornix. , 1974, Journal of comparative and physiological psychology.

[4]  M Mishkin,et al.  An analysis of short-term visual memory in the monkey. , 1975, Journal of experimental psychology. Animal behavior processes.

[5]  R. F. Thompson,et al.  Neuronal substrate of classical conditioning in the hippocampus , 1976, Science.

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

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

[8]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

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

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

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

[12]  J. M. Novak,et al.  Serial position curve in rats: role of the dorsal hippocampus. , 1982, Science.

[13]  L. Voronin,et al.  Long-term potentiation in the hippocampus , 1983, Neuroscience.

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

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

[16]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

[17]  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.

[18]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[19]  G. Preti,et al.  Carbon disulfide: A semiochemical mediating socially-induced diet choice in rats , 1988, Physiology & Behavior.

[20]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[21]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  H. Eichenbaum,et al.  Spatial and behavioral correlates of hippocampal neuronal activity. , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[24]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

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

[26]  H. Eichenbaum,et al.  Hippocampal representation in place learning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  Tim Shallice,et al.  Neuropsychological impairments of short-term memory , 1992 .

[28]  L. F. Kromer,et al.  Object recognition memory in the rat: the role of the hippocampus , 1991, Behavioural Brain Research.

[29]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[30]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task , 1992 .

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

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

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

[34]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. , 1992, Behavioral neuroscience.

[35]  Joseph E LeDoux Brain mechanisms of emotion and emotional learning , 1992, Current Biology.

[36]  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.

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

[38]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

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

[40]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[42]  J. Fuster Memory in the cerebral cortex , 1994 .

[43]  R. Muller,et al.  On the directional firing properties of hippocampal place cells , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Michael Davis,et al.  The role of the amygdala in emotional learning. , 1994, International review of neurobiology.

[45]  D. Gaffan Scene-Specific Memory for Objects: A Model of Episodic Memory Impairment in Monkeys with Fornix Transection , 1994, Journal of Cognitive Neuroscience.

[46]  James L. McGaugh,et al.  The amygdala and emotional memory , 1995, Nature.

[47]  L. Squire,et al.  Retrograde amnesia and memory consolidation: a neurobiological perspective , 1995, Current Opinion in Neurobiology.

[48]  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.

[49]  H Eichenbaum,et al.  Selective damage to the hippocampal region blocks long‐term retention of a natural and nonspatial stimulus‐stimulus association , 1995, Hippocampus.

[50]  D. Salmon,et al.  Neurobiology of skill and habit learning , 1995, Current Opinion in Neurobiology.

[51]  J J Kim,et al.  Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. , 1995, Behavioral neuroscience.

[52]  Richard F. Thompson,et al.  Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. , 1995, Behavioral neuroscience.

[53]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  H. Eichenbaum,et al.  On the Binding of Associations in Memory: Clues From Studies on the Role of the Hippocampal Region in Paired-Associate Learning , 1995 .

[55]  J. D. Nichols,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. , 1997, Science.

[56]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[57]  H. Cassaday,et al.  Fornix-fimbria section and working memory deficits in rats: stimulus complexity and stimulus size. , 1995, Behavioral neuroscience.

[58]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain , 1995, Hippocampus.

[59]  R. Adolphs,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans , 1995, Science.

[60]  Richard B. Ivry,et al.  Cerebellar involvement in eyeblink classical conditioning in humans. , 1996 .

[61]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[62]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[63]  R. Muller,et al.  A Quarter of a Century of Place Cells , 1996, Neuron.

[64]  Gurindar S. Sohi,et al.  Memory systems , 1996, CSUR.

[65]  S. Wise,et al.  The Acquisition of Motor Behavior in Vertebrates , 1996 .

[66]  E. Warrington Studies of retrograde memory: a long-term view. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[67]  H. Eichenbaum,et al.  Conservation of hippocampal memory function in rats and humans , 1996, Nature.

[68]  Wendy A. Suzuki,et al.  Neuroanatomy of the monkey entorhinal, perirhinal and parahippocampal cortices: Organization of cortical inputs and interconnections with amygdala and striatum , 1996 .

[69]  Y. Miyashita,et al.  Formation of mnemonic neuronal responses to visual paired associates in inferotemporal cortex is impaired by perirhinal and entorhinal lesions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[70]  J. D. McGaugh,et al.  Involvement of the amygdala in memory storage: interaction with other brain systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[71]  K M Gothard,et al.  Dynamics of Mismatch Correction in the Hippocampal Ensemble Code for Space: Interaction between Path Integration and Environmental Cues , 1996, The Journal of Neuroscience.

[72]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[73]  N. White Mnemonic functions of the basal ganglia , 1997, Current Opinion in Neurobiology.

[74]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[75]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

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

[77]  H Eichenbaum,et al.  Declarative memory: insights from cognitive neurobiology. , 1997, Annual review of psychology.

[78]  H. Eichenbaum,et al.  The hippocampus and memory for orderly stimulus relations. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[79]  H. Eichenbaum,et al.  Memory Representation within the Parahippocampal Region , 1997, The Journal of Neuroscience.

[80]  Larry R. Squire,et al.  MEMORY SYSTEMS OF THE BRAIN , 1997 .

[81]  D. Amaral,et al.  Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat , 1998 .

[82]  A. Dickinson,et al.  Episodic-like memory during cache recovery by scrub jays , 1998, Nature.

[83]  M. W. Brown,et al.  Recognition memory: neuronal substrates of the judgement of prior occurrence , 1998, Progress in Neurobiology.

[84]  E. Kandel,et al.  Cognitive Neuroscience and the Study of Memory , 1998, Neuron.

[85]  L R Squire,et al.  Retrograde Amnesia for Facts and Events: Findings from Four New Cases , 1998, The Journal of Neuroscience.

[86]  M. Hasselmo,et al.  The hippocampus as an associator of discontiguous events , 1998, Trends in Neurosciences.

[87]  L. Squire,et al.  Episodic memory, semantic memory, and amnesia , 1998, Hippocampus.

[88]  M. Mishkin,et al.  Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus , 1998, The Journal of Neuroscience.

[89]  M. Chun,et al.  Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage , 1999, Nature Neuroscience.

[90]  Robert E. Hampson,et al.  Distribution of spatial and nonspatial information in dorsal hippocampus , 1999, Nature.

[91]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[92]  Malcolm W. Brown,et al.  Different Contributions of the Hippocampus and Perirhinal Cortex to Recognition Memory , 1999, The Journal of Neuroscience.

[93]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[94]  E. Miller,et al.  The Prefrontal Cortex Complex Neural Properties for Complex Behavior , 1999, Neuron.

[95]  Larry R. Squire,et al.  Memory for places learned long ago is intact after hippocampal damage , 1999, Nature.

[96]  A. Diantonio Learning Something ORIGINal at the Drosophila Neuromuscular Junction , 1999, Neuron.

[97]  T. Bussey,et al.  Perceptual–mnemonic functions of the perirhinal cortex , 1999, Trends in Cognitive Sciences.

[98]  Seth J. Ramus,et al.  Dissociation between the effects of damage to perirhinal cortex and area TE. , 1999, Learning & memory.

[99]  J. Lisman Relating Hippocampal Circuitry to Function Recall of Memory Sequences by Reciprocal Dentate–CA3 Interactions , 1999, Neuron.

[100]  H. Eichenbaum,et al.  The global record of memory in hippocampal neuronal activity , 1999, Nature.

[101]  R. Morris,et al.  Delay‐dependent impairment of a matching‐to‐place task with chronic and intrahippocampal infusion of the NMDA‐antagonist D‐AP5 , 1999, Hippocampus.

[102]  R. Clark,et al.  Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region , 2000, The Journal of Neuroscience.

[103]  H. Eichenbaum,et al.  The Neurophysiology of Memory , 2000, Annals of the New York Academy of Sciences.

[104]  E. Rolls,et al.  Memory systems in the brain. , 2000, Annual review of psychology.

[105]  H. Eichenbaum,et al.  Hippocampal Neurons Encode Information about Different Types of Memory Episodes Occurring in the Same Location , 2000, Neuron.

[106]  H Eichenbaum,et al.  Neural Correlates of Olfactory Recognition Memory in the Rat Orbitofrontal Cortex , 2000, The Journal of Neuroscience.

[107]  J. Goodhouse,et al.  Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice , 2000, Nature Neuroscience.

[108]  N. Cohen From Conditioning to Conscious Recollection Memory Systems of the Brain. Oxford Psychology Series, Volume 35. , 2001 .

[109]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

[110]  Richard Horn,et al.  Learning and Retention of Pattern-Analyzing Skill in Amnesia : Dissociation of Knowing How and Knowing That , 2022 .