Integrating behavioral and physiological models of hippocampal function

In recent modeling of hippocampal function, we have attempted to integrate formal behavioral analyses of classical conditioning with psychobiological data on brain lesions (Gluck and Myers [1993] Hippocampus 3:491–516; Myers and Gluck [1994] Behav Neurosci 108(5):835–847). Based on comparative behavioral analyses, we have argued that animals with hippocampal region damage are unable to alter stimulus similarity based on experience. While hippocampal‐damaged animals can still learn whether to respond to an individual stimulus, they are notably impaired at many tasks involving learning relationships between stimuli—especially in the absence of explicit reinforcement. These analyses lead to a computational theory which identifies two representational recoding processes—predictive differentiation and redundancy compression—which alter stimulus similarity relationships in intact animals but are dependent on intact hippocampal region processing. More recent, and ongoing, modeling aims to broaden this model of hippocampal region function in classical conditioning, with an emphasis on physiological and anatomical constraints, including the role of the fornix and subcortical modulation, preprocessing in sensory cortices, and localization of the proposed representational functions within more precisely identified hippocampal region substrates (Myers et al. [1995] Psychology 23(2):116–138; Myers and Gluck [1996] Behav Neurosci; Myers et al. [1996] Neurobiol Learning Memory). Working to bridge between behavioral and physiological levels of analysis, we ultimately hope to develop a more complete understanding of hippocampal region function in memory across a wider range of behavioral paradigms, elucidating how this functionality emerges from underlying physiological and anatomical substrates. © 1997 Wiley‐Liss, Inc.

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

[2]  N. Mackintosh,et al.  Mechanisms of animal discrimination learning , 1971 .

[3]  J. Theios,et al.  Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). , 1972, Journal of comparative and physiological psychology.

[4]  R. Rescorla,et al.  A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement , 1972 .

[5]  R. Lubow Latent inhibition. , 1973, Psychological bulletin.

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

[7]  P. Solomon,et al.  Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. , 1975, Journal of comparative and physiological psychology.

[8]  JOHN W. Moore,et al.  Central cholinergic blockade by scopolamine and habituation, classical conditioning, and latent inhibition of the rabbit’s nictitating membrane response , 1976 .

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

[10]  S. D. Berry,et al.  Medial septal lesions retard classical conditioning of the nicitating membrane response in rabbits. , 1979, Science.

[11]  J. O’Keefe A review of the hippocampal place cells , 1979, Progress in Neurobiology.

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

[13]  J. Pearce,et al.  A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. , 1980, Psychological review.

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

[15]  J. Pearce,et al.  A model for Pavlovian learning: Variations in the effectiveness of conditioned but not of unconditioned stimuli. , 1980 .

[16]  A. Dickinson Conditioning and associative learning. , 1981, British medical bulletin.

[17]  Emotional factors involved in classical conditioning of the nictitating membrane response in rabbits , 1982, Behavioural Brain Research.

[18]  W. B. Orr,et al.  Hippocampectomy selectively disrupts discrimination reversal conditioning of the rabbit nictitating membrane response , 1983, Behavioural Brain Research.

[19]  P. Solomon,et al.  Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. , 1983, Science.

[20]  W. Levy,et al.  Partial quantification of the associative synaptic learning rule of the dentate gyrus , 1983, Neuroscience.

[21]  M. M. Patterson,et al.  Fimbrial lesions and sensory preconditioning. , 1984, Behavioral neuroscience.

[22]  David Zipser,et al.  Feature Discovery by Competive Learning , 1986, Cogn. Sci..

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

[24]  R. Morris,et al.  Allocentric Spatial Learning by Hippocampectomised Rats: A Further Test of the “Spatial Mapping” and “Working Memory” Theories of Hippocampal Function , 1986, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[25]  J. Pearce,et al.  Hippocampal Lesions Attenuate Latent Inhibition and the Decline of the Orienting Response in Rats , 1987, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

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

[27]  Richard F. Thompson The neural basis of basic associative learning of discrete behavioral responses , 1988, Trends in Neurosciences.

[28]  H. Eichenbaum,et al.  Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. , 1988, Behavioral neuroscience.

[29]  I. Daum,et al.  Classical conditioning in patients with severe memory problems. , 1989, Journal of neurology, neurosurgery, and psychiatry.

[30]  H Eichenbaum,et al.  Further studies of hippocampal representation during odor discrimination learning. , 1989, Behavioral neuroscience.

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

[32]  G. Lynch,et al.  The neurobiology of learning and memory , 1989, Cognition.

[33]  R. F. Thompson,et al.  Neural mechanisms of classical conditioning in mammals. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  Acquisition of classically conditioned-related activity in the hippocampus is affected by lesions of the cerebellar interpositus nucleus. , 1990 .

[35]  Geoffrey E. Hinton 20 – CONNECTIONIST LEARNING PROCEDURES1 , 1990 .

[36]  J Ambros-Ingerson,et al.  Simulation of paleocortex performs hierarchical clustering. , 1990, Science.

[37]  I. Weiner Neural substrates of latent inhibition: the switching model. , 1990, Psychological bulletin.

[38]  J. Steinmetz,et al.  Acquisition of classically conditioned-related activity in the hippocampus is affected by lesions of the cerebellar interpositus nucleus. , 1990, Behavioral neuroscience.

[39]  T. Otto,et al.  Analysis of aversively conditioned learning and memory in rats recovered from pyrithiamine-induced thiamine deficiency. , 1991, Behavioral neuroscience.

[40]  J S Taube,et al.  Space, the final hippocampal frontier? , 1991, Hippocampus.

[41]  Y. Miyashita,et al.  Neural organization for the long-term memory of paired associates , 1991, Nature.

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

[43]  P. Solomon,et al.  Hippocampus, context, and conditioning. , 1991, Behavioral neuroscience.

[44]  Hippocampus, context, and conditioning. , 1991, Behavioral neuroscience.

[45]  G. Lynch,et al.  Hippocampus and olfactory discrimination learning: effects of entorhinal cortex lesions on olfactory learning and memory in a successive-cue, go-no-go task. , 1991, Behavioral neuroscience.

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

[47]  B. McNaughton,et al.  Dead Reckoning, Landmark Learning, and the Sense of Direction: A Neurophysiological and Computational Hypothesis , 1991, Journal of Cognitive Neuroscience.

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

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

[50]  E T Rolls,et al.  Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network , 1992, Hippocampus.

[51]  Bryan J. Travis,et al.  A Computational Model of the Cerebellum , 1992 .

[52]  D. Woodruff-Pak,et al.  Eyeblink classical conditioning in H.M.: delay and trace paradigms. , 1993, Behavioral neuroscience.

[53]  P. Solomon,et al.  Disruption of human eyeblink conditioning after central cholinergic blockade with scopolamine. , 1993, Behavioral neuroscience.

[54]  C. Harley,et al.  Ibotenate lesions of the hippocampus enhance latent inhibition in conditioned taste aversion and increase resistance to extinction in conditioned taste preference. , 1993, Behavioral neuroscience.

[55]  E. Rolls,et al.  Modification of the responses of hippocampal neurons in the monkey during the learning of a conditional spatial response task , 1993, Hippocampus.

[56]  D. Woodruff-Pak,et al.  Delay classical conditioning in young and older rabbits: initial acquisition and retention at 12 and 18 months. , 1993, Behavioral neuroscience.

[57]  H Eichenbaum,et al.  Critical role of the parahippocampal region for paired-associate learning in rats. , 1993, Behavioral neuroscience.

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

[59]  M A Gluck,et al.  Computational models of the neural bases of learning and memory. , 1993, Annual review of neuroscience.

[60]  E. Macphail,et al.  Lateral hyperstriatal lesions disrupt simultaneous but not successive conditional discrimination learning of pigeons (Columba livia). , 1993, Behavioral neuroscience.

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

[62]  R. C. Honey,et al.  Selective hippocampal lesions abolish the contextual specificity of latent inhibition and conditioning. , 1993, Behavioral neuroscience.

[63]  M. Gluck,et al.  A computational perspective on dissociating hippocampal and entorhinal function , 1994, Behavioral and Brain Sciences.

[64]  G. Lynch,et al.  Memory: Organization and locus of change , 1994 .

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

[66]  J. Gray,et al.  Psychoarithmetic or pick your own? , 1994, Behavioral and Brain Sciences.

[67]  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.

[68]  M. Gluck,et al.  Context, conditioning, and hippocampal rerepresentation in animal learning. , 1994, Behavioral neuroscience.

[69]  M. Hasselmo,et al.  Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3 , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  M. Hasselmo,et al.  Feedback Regulation of Cholinergic Modulation and Hippocampal Memory Function , 1995 .

[71]  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.

[72]  J W Rudy,et al.  A comparison of kainic acid plus colchicine and ibotenic acid-induced hippocampal formation damage on four configural tasks in rats. , 1995, Behavioral neuroscience.

[73]  M. Gluck,et al.  Representation and Association in Memory: A Neurocomputational View of Hippocampal Function , 1995 .

[74]  M. Gluck,et al.  Dissociation of hippocampal and entorhinal function in associative learning: A computational approach , 1995, Psychobiology.

[75]  M. Gluck,et al.  Intact delay-eyeblink classical conditioning in amnesia. , 1995, Behavioral neuroscience.

[76]  M. Hasselmo,et al.  A Computational Model of Cholinergic Disruption of Septohippocampal Activity in Classical Eyeblink Conditioning , 1996, Neurobiology of Learning and Memory.

[77]  C. Buhusi,et al.  Attention, configuration, and hippocampal function , 1996, Hippocampus.

[78]  M. Gluck,et al.  Cortico-hippocampal representations in simultaneous odor discrimination: a computational interpretation of Eichenbaum, Mathews, and Cohen (1989). , 1996, Behavioral neuroscience.

[79]  J. Murre TraceLink: A model of amnesia and consolidation of memory , 1996, Hippocampus.

[80]  M. Hasselmo,et al.  Encoding and retrieval of episodic memories: Role of cholinergic and GABAergic modulation in the hippocampus , 1998, Hippocampus.

[81]  James L. McClelland,et al.  Considerations arising from a complementary learning systems perspective on hippocampus and neocortex , 1996, Hippocampus.