Complementary Learning Systems 1 Why there are Complementary Learning Systems in the Hippocampus and Neocortex : Insights from the Successes and Failures of Connectionist Models of Learning and Memory

Damage to the hippocampal system disrupts recent memory but leaves remote memory intact. Our account of this suggests that memories are first stored via synaptic changes in the hippocampal system; that these changes support reinstatement of recent memories in the neocortex; that neocortical synapses change a little on each reinstatement; and that remote memory is based on accumulated neocortical changes. Models that learn via adaptive changes to connections help explain this organization. These models discover the structure in ensembles of items if learning of each item is gradual and interleaved with learning about other items. This suggests that neocortex learns slowly to discover the structure in ensembles of experiences. The hippocampal system permits rapid learning of new items without disrupting this structure, and reinstatement of new memories interleaves them with others to integrate them into structured neocortical memory systems. Psychological Review, in press

[1]  James L. McClelland,et al.  Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off , 1994, Hippocampus.

[2]  L. Jarrard On the role of the hippocampus in learning and memory in the rat. , 1993, Behavioral and neural biology.

[3]  Geoffrey E. Hinton,et al.  Learning internal representations by error propagation , 1986 .

[4]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[5]  Bruce L. McNaughton,et al.  Hippocampal Place Fields, the Internal Compass, and the Learning of Landmark Stability, , 1994 .

[6]  Wendy A. Suzuki,et al.  What can neuroanatomy tell us about the functional components of the hippocampal memory system? , 1994, Behavioral and Brain Sciences.

[7]  B. Milner,et al.  Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M.☆ , 1968 .

[8]  David S. Touretzky,et al.  A distributed connectionist representation for concept structures , 1987 .

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

[10]  M. Ross Quillian,et al.  Retrieval time from semantic memory , 1969 .

[11]  Daniel L. Schacter,et al.  Priming and Multiple Memory Systems: Perceptual Mechanisms of Implicit Memory , 1992, Journal of Cognitive Neuroscience.

[12]  Larry R. Squire,et al.  Forgetting in very long-term memory as assessed by an improved questionnaire technique. , 1975 .

[13]  James L. McClelland,et al.  Distributed memory and the representation of general and specific information. , 1985, Journal of experimental psychology. General.

[14]  R Linsker,et al.  From basic network principles to neural architecture: emergence of spatial-opponent cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[15]  G. Lynch,et al.  Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. , 1986, Science.

[16]  B. Milner Amnesia following operation on the temporal lobes , 1996 .

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

[18]  L. Squire,et al.  Memory and amnesia: resistance to disruption develops for years after learning. , 1979, Behavioral and neural biology.

[19]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[20]  G Mandler,et al.  The information that amnesic patients do not forget. , 1984, Journal of experimental psychology. Learning, memory, and cognition.

[21]  D. Schacter,et al.  Modality specificity of implicit memory for new associations. , 1989 .

[22]  C. Barnes Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat , 1988, Trends in Neurosciences.

[23]  B L McNaughton,et al.  Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Stephen Grossberg,et al.  Competitive Learning: From Interactive Activation to Adaptive Resonance , 1987, Cogn. Sci..

[25]  G. Collingridge,et al.  Excitatory amino acids in synaptic transmission in the Schaffer collateral‐commissural pathway of the rat hippocampus. , 1983, The Journal of physiology.

[26]  R Linsker,et al.  From basic network principles to neural architecture: emergence of orientation columns. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

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

[28]  Robert M. French,et al.  Using Semi-Distributed Representations to Overcome Catastrophic Forgetting in Connectionist Networks , 1991 .

[29]  W. James Psychology: Briefer Course , 2020 .

[30]  L. Squire,et al.  The learning of categories: parallel brain systems for item memory and category knowledge. , 1993, Science.

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

[32]  John E. Moody,et al.  Note on Learning Rate Schedules for Stochastic Optimization , 1990, NIPS.

[33]  Seth J. Ramus,et al.  Intact Artificial Grammar Learning in Amnesia: Dissociation of Classification Learning and Explicit Memory for Specific Instances , 1992 .

[34]  K. Miller,et al.  Ocular dominance column development: analysis and simulation. , 1989, Science.

[35]  E Tulving,et al.  Learning and retention of computer-related vocabulary in memory-impaired patients: method of vanishing cues. , 1986, Journal of clinical and experimental neuropsychology.

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

[37]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[38]  B. L. McNaughton,et al.  Suppression of hippocampal synaptic plasticity during slow-wave sleep , 1987, Brain Research.

[39]  B. McNaughton,et al.  Hebb-Marr networks and the neurobiological representation of action in space. , 1990 .

[40]  Robert M. French,et al.  Semi-distributed Representations and Catastrophic Forgetting in Connectionist Networks , 1992 .

[41]  Antonio R. Damasio,et al.  The Brain Binds Entities and Events by Multiregional Activation from Convergence Zones , 1989, Neural Computation.

[42]  D. Amaral,et al.  Memory and the Hippocampus , 1989 .

[43]  Geoffrey E. Hinton,et al.  A Learning Algorithm for Boltzmann Machines , 1985, Cogn. Sci..

[44]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[45]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Michael I. Jordan,et al.  A more biologically plausible learning rule for neural networks. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[47]  H. Wigström,et al.  Mode of action of excitatory amino acid receptor antagonists on hippocampal long-lasting potentiation , 1986, Neuroscience.

[48]  B L McNaughton,et al.  LTP saturation and spatial learning disruption: effects of task variables and saturation levels , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  David E. Rumelhart,et al.  Brain style computation: learning and generalization , 1990 .

[50]  W. Levy A computational approach to hippocampal function , 1989 .

[51]  Geoffrey E. Hinton,et al.  Learning distributed representations of concepts. , 1989 .

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

[53]  Geoffrey E. Hinton,et al.  Deterministic Boltzmann Learning in Networks with Asymmetric Connectivity , 1991 .

[54]  Wayne A. Wickelgren,et al.  Trace resistance and the decay of long-term memory. , 1972 .

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

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

[57]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[58]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[59]  D L Schacter,et al.  Preserved learning in amnesic patients: perspectives from research on direct priming. , 1986, Journal of clinical and experimental neuropsychology.

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

[61]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[62]  Peter M. Todd,et al.  Learning and connectionist representations , 1993 .

[63]  D. Marr A theory for cerebral neocortex , 1970, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[64]  D. Lavond Cellular and molecular mechanisms underlying higher neural functions edited by A.I. Selverston and P. Ascher, John Wiley & Sons, 1994. £65.00 (328 pages) ISBN 0 471 94304 5 , 1995, Trends in Neurosciences.

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

[66]  Axel Cleeremans,et al.  Mechanisms of Implicit Learning: Connectionist Models of Sequence Processing , 1993 .

[67]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[68]  R Ratcliff,et al.  Connectionist models of recognition memory: constraints imposed by learning and forgetting functions. , 1990, Psychological review.

[69]  M. McKERNAN,et al.  Hippocampal lesions do not impair negative patterning: a challenge to configural association theory. , 1993, Behavioral neuroscience.

[70]  G. Buzsáki,et al.  Selective activation of deep layer (V-VI) retrohippocampal cortical neurons during hippocampal sharp waves in the behaving rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[72]  James L. McClelland,et al.  State-Dependent Factors Influencing Neural Plasticity: A Partial Account of the Critical Period , 1987 .

[73]  E. Rolls Principles underlying the representation and storage of information in neuronal networks in the primate hippocampus and cerebral cortex , 1990 .

[74]  G. Buzsáki Two-stage model of memory trace formation: A role for “noisy” brain states , 1989, Neuroscience.

[75]  M. L. Howe,et al.  On resolving the enigma of infantile amnesia. , 1993, Psychological bulletin.

[76]  G. Lynch,et al.  Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5 , 1986, Nature.

[77]  T. Teyler,et al.  The hippocampal memory indexing theory. , 1986, Behavioral neuroscience.

[78]  Daniel L. Schacter,et al.  Computer learning by memory-impaired patients: Acquisition and retention of complex knowledge , 1986, Neuropsychologia.

[79]  B. Underwood,et al.  Fate of first-list associations in transfer theory. , 1959, Journal of experimental psychology.

[80]  B. McNaughton,et al.  Reactivation of hippocampal ensemble memories during sleep. , 1994, Science.

[81]  B L McNaughton,et al.  An age comparison of the rates of acquisition and forgetting of spatial information in relation to long-term enhancement of hippocampal synapses. , 1985, Behavioral neuroscience.

[82]  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.

[83]  R Linsker,et al.  From basic network principles to neural architecture: emergence of orientation-selective cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[84]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  Bruce L. McNaughton,et al.  Why do we have a special learning system in the hippocampus?,(Abstract 580) , 1993 .

[86]  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.

[87]  B. McNaughton,et al.  Hippocampal synaptic enhancement and information storage within a distributed memory system , 1987, Trends in Neurosciences.

[88]  L R Squire,et al.  Impaired priming of new associations in amnesia. , 1989, Journal of experimental psychology. Learning, memory, and cognition.

[89]  C. Pavlides,et al.  Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  J. Haldane The interaction of nature and nurture. , 1946, Annals of eugenics.

[91]  D. Schacter Implicit memory: History and current status. , 1987 .

[92]  D. Marr A theory of cerebellar cortex , 1969, The Journal of physiology.

[93]  Lance J. Rips,et al.  Semantic distance and the verification of semantic relations , 1973 .

[94]  B. McNaughton,et al.  Cortical-hippocampal interactions and cognitive mapping: A hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing , 1989 .

[95]  C. Barnes Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. , 1979, Journal of comparative and physiological psychology.

[96]  L. Jarrard On the use of ibotenic acid to lesion selectively different components of the hippocampal formation , 1989, Journal of Neuroscience Methods.

[97]  William B. Levy,et al.  Predicting Complex Behavior in Sparse Asymmetric Networks , 1992, NIPS.

[98]  M. Humphreys,et al.  Different Ways to Cue a Coherent Memory System: A Theory for Episodic, Semantic, and Procedural Tasks. , 1989 .

[99]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[100]  P Alvarez,et al.  Memory consolidation and the medial temporal lobe: a simple network model. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[101]  James L. McClelland,et al.  Explorations in parallel distributed processing: a handbook of models, programs, and exercises , 1988 .

[102]  D. Schacter,et al.  Selective effects of interference on implicit and explicit memory for new associations. , 1987 .

[103]  L R Squire,et al.  A neuropsychological study of fact memory and source amnesia. , 1987, Journal of experimental psychology. Learning, memory, and cognition.

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

[105]  D L Schacter,et al.  Implicit memory and test awareness. , 1990, Journal of experimental psychology. Learning, memory, and cognition.

[106]  Geoffrey E. Hinton,et al.  Learning Representations by Recirculation , 1987, NIPS.

[107]  Stephen José Hanson,et al.  Connectionist modeling and brain function : the developing interface , 1990 .

[108]  Larry R. Squire,et al.  Functional distinctions within the medical temporal lobe memory system: What is the evidence? , 1994, Behavioral and Brain Sciences.

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

[110]  C. Stewart,et al.  Electroconvulsive stimulation and synaptic plasticity in the rat , 1993, Brain Research.

[111]  N. Schmajuk,et al.  Stimulus configuration, classical conditioning, and hippocampal function. , 1992, Psychological review.

[112]  Jonathan D. Cohen,et al.  A preliminary theory of the interactions between prefrontal cortex and hippocampus that contribute to planning and prospective memory. , 1996 .

[113]  Regional variations in NMDA receptor properties—evidence for receptor isoforms Daniel T. Monaghan, University of Nebraska Medical Center, Omaha, NE 68198-6260 U.S.A. , 1990, Neurochemistry International.

[114]  John Garcia,et al.  Learning with prolonged delay of reinforcement , 1966 .

[115]  K. McRae,et al.  Catastrophic Interference is Eliminated in Pretrained Networks , 1993 .

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

[117]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[118]  G. Recanzone,et al.  Adaptive mechanisms in cortical networks underlying cortical contributions to learning and nondeclarative memory. , 1990, Cold Spring Harbor symposia on quantitative biology.

[119]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[120]  Teuvo Kohonen,et al.  Self-Organization and Associative Memory , 1988 .

[121]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[122]  E. Warrington,et al.  Further analysis of the prior learning effect in amnesic patients , 1978, Neuropsychologia.

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

[124]  Gordon H. Bower,et al.  Computational models of learning in simple neural systems , 1989 .

[125]  E. Murray,et al.  Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations. , 1992, Behavioral neuroscience.

[126]  Halbert White,et al.  Learning in Artificial Neural Networks: A Statistical Perspective , 1989, Neural Computation.

[127]  R. Muller,et al.  The firing of hippocampal place cells in the dark depends on the rat's recent experience , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[128]  L. Squire,et al.  Intact priming of words and nonwords in amnesia , 1991, Psychobiology.

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

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

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

[132]  R. Schmidt,et al.  New Conceptualizations of Practice: Common Principles in Three Paradigms Suggest New Concepts for Training , 1992 .

[133]  Michael McCloskey,et al.  Catastrophic Interference in Connectionist Networks: The Sequential Learning Problem , 1989 .

[134]  James L. McClelland,et al.  Understanding normal and impaired word reading: computational principles in quasi-regular domains. , 1996, Psychological review.

[135]  M. Gluck,et al.  Hippocampal mediation of stimulus representation: A computational theory , 1993, Hippocampus.