Hebb, Pandemonium and Catastrophic Hypermnesia: The Hippocampus as a Suppressor of Inappropriate Associations

The hippocampus has been proposed as a key component of a "behavioural inhibition system". We explore the implications of this idea for the nature of associative memory--i.e. learning that is distinct from the moulding of response sequences by error correction and reinforcement. It leads to the view that all associative memory depends on purely Hebbian mechanisms. Memories involve acquisition of new goals not the strengthening of new stimulus-response links. Critically, memories will consist of affectively positive and affectively negative associations as well "purely cognitive" information. The hippocampus is seen as a supervisor that is normally "just checking" information about current available goals. When one available goal is pre-eminent there is no hippocampal output and the goal controls the response system. When two or more goals are similarly and highly primed there is conflict. This is detected by the hippocampus which sends output that increases the valence of affectively negative perceptions and so resolves the conflict by suppressing more aversive goals. Such conflict resolution occurs with innate as well as acquired goals and is fundamentally non-memorial. But, in memory paradigms, it can often act to suppress interference on the current trial and, through Hebbian association of the increase in negative affect, decrease the probability of interference on later trials and during consolidation. Both memory-driven and innate behaviour is made hippocampal-dependent by innate and acquired conflicting tendencies and not the class of stimulus presented.

[1]  G. Winocur,et al.  Hippocampus and septum in response inhibition. , 1969, Journal of comparative and physiological psychology.

[2]  N. McNaughton,et al.  Common Firing Patterns of Hippocampal Cells in a Differential Reinforcement of Low Rates of Response Schedule , 2000, The Journal of Neuroscience.

[3]  A. Amsel,et al.  THE INFLUENCE OF MAGNITUDE OF REWARD ON THE AVERSIVE PROPERTIES OF ANTICIPATORY FRUSTRATION. , 1964, Canadian journal of psychology.

[4]  J. Gray Drug Effects on Fear and Frustration: Possible Limbic Site of Action of Minor Tranquilizers , 1977 .

[5]  Morris Moscovitch,et al.  Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions , 2000, Nature Neuroscience.

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

[7]  N. McNaughton Cognitive Dysfunction Resulting from Hippocampal Hyperactivity—A Possible Cause of Anxiety Disorder? , 1997, Pharmacology Biochemistry and Behavior.

[8]  H. Okaichi,et al.  Effects of fimbria-fornix lesions on avoidance tasks with temporal elements in rats , 1994, Physiology & Behavior.

[9]  R. Deacon,et al.  Critical determinants of nonspatial working memory deficits in rats with conventional lesions of the hippocampus or fornix. , 1993, Behavioral neuroscience.

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

[11]  J. Gray,et al.  Précis of The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system , 1982, Behavioral and Brain Sciences.

[12]  J. Gray,et al.  The psychophysiological basis of introversion-extraversion. , 1970, Behaviour research and therapy.

[13]  B. McNaughton,et al.  Replay of Neuronal Firing Sequences in Rat Hippocampus During Sleep Following Spatial Experience , 1996, Science.

[14]  J. Gabrieli A systematic view of human memory processes , 1995, Journal of the International Neuropsychological Society.

[15]  A. Amsel,et al.  Frustration theory and partial reinforcement effects: the acquisition-extinction paradox. , 1969, Psychological review.

[16]  K. Doya Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[17]  E. Warrington,et al.  The effect of prior learning on subsequent retention in amnesic patients. , 1974, Neuropsychologia.

[18]  S. Iversen,et al.  Handbook of Psychopharmacology , 1988, Springer US.

[19]  L Weiskrantz,et al.  A comparison of hippocampal pathology in man and other animals. , 1977, Ciba Foundation symposium.

[20]  A. Benton,et al.  Frontal Lobe Function and Dysfunction , 1991 .

[21]  Barbara A. Wilson,et al.  When implicit learning fails: Amnesia and the problem of error elimination , 1994, Neuropsychologia.

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

[23]  W. F. Prokasy,et al.  Classical conditioning II: Current research and theory. , 1972 .

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

[25]  W. K. Honig,et al.  Cognitive Processes in Animal Behavior , 1979 .

[26]  R. O’Reilly,et al.  Computational principles of learning in the neocortex and hippocampus , 2000, Hippocampus.

[27]  P. Goldman-Rakic Working memory and the mind. , 1992, Scientific American.

[28]  E. Rolls,et al.  Hippocampo‐cortical and cortico‐cortical backprojections , 2000, Hippocampus.

[29]  R. Isaacson,et al.  Hippocampal lesions and the frustration effects in rats. , 1969, Journal of comparative and physiological psychology.

[30]  N. Mackintosh The psychology of animal learning , 1974 .

[31]  R. G. Morris D.O. Hebb: The Organization of Behavior, Wiley: New York; 1949 , 1999, Brain Research Bulletin.

[32]  L. Nadel,et al.  Multiple trace theory of human memory: Computational, neuroimaging, and neuropsychological results , 2000, Hippocampus.

[33]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[34]  J. Gray,et al.  The psychology of fear and stress , 1971 .

[35]  Norman Abeles,et al.  The Corsini encyclopedia of psychology and behavioral science , 2001 .

[36]  C. L. Hull,et al.  A Behavior System , 1954 .

[37]  T. Robbins,et al.  Refining the Taxonomy of Memory , 1996, Science.

[38]  James M. Bower,et al.  Acetylcholine and memory , 1993, Trends in Neurosciences.

[39]  J. Gray,et al.  Pavlovian Counterconditioning is Unchanged by Chlordiazepoxide or by Septal Lesions , 1983, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[40]  A. Amsel,et al.  Motivational properties of frustration. I. Effect on a running response of the addition of frustration to the motivational complex. , 1952, Journal of experimental psychology.

[41]  N. McNaughton Is the hippocampus a store, intermediate or otherwise? , 1985, Behavioral and Brain Sciences.

[42]  D. Shanks,et al.  Characteristics of dissociable human learning systems , 1994, Behavioral and Brain Sciences.

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

[44]  E. Warrington,et al.  Verbal learning and retention by amnesic patients using partial information , 1970 .

[45]  N. McNaughton,et al.  Comparison between the behavioural effects of septal and hippocampal lesions: A review , 1983, Neuroscience & Biobehavioral Reviews.

[46]  D. O. Hebb,et al.  The organization of behavior , 1988 .

[47]  C. Beer The Oxford companion to animal behavior , 1983 .

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

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

[50]  P. Wong,et al.  Transfer of persistence from fixed-ratio barpress training to runway extinction , 1976 .

[51]  A. Baddeley Human Memory: Theory and Practice, Revised Edition , 1990 .

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

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

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

[55]  J. Rawlins,et al.  The effects of hippocampectomy and of fimbria section upon the partial reinforcement extinction effect in rats , 1980, Experimental Brain Research.

[56]  L. Squire Declarative and Nondeclarative Memory: Multiple Brain Systems Supporting Learning and Memory , 1992, Journal of Cognitive Neuroscience.

[57]  Review of Elements of episodic memory. , 1985 .

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

[59]  Joseph E LeDoux Emotion, memory and the brain. , 1994, Scientific American.

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

[61]  L. Squire,et al.  The Neuropsychology of Memory: New Links between Humans and Experimental Animals , 1985, Annals of the New York Academy of Sciences.

[62]  A. Black Functions of the septo-hippocampal system , 1978, Nature.

[63]  J. W. Papez A PROPOSED MECHANISM OF EMOTION , 1937 .

[64]  A. Amsel Frustration Theory: An Analysis of Dispositional Learning and Memory , 1992 .

[65]  M. Page,et al.  Connectionist modelling in psychology: A localist manifesto , 2000, Behavioral and Brain Sciences.

[66]  R. Kesner,et al.  Dissociation of data-based and expectancy-based memory following hippocampal lesions in rats. , 1988, Behavioral and neural biology.

[67]  Dr. Robert Miller Cortico-Hippocampal Interplay and the Representation of Contexts in the Brain , 1991, Studies of Brain Function.