The Hippocampal System and Declarative Memory in Animals

Theoretical arguments and empirical data are presented in favor of the hypothesis that the hippocampal system supports a declarative memory capacity in animals as well as humans. This view is advanced by identifying two prominent characteristics of human declarative memory and by operationalizing and evaluating them using both experimental lesion and single unit recording studies on animals. First, hippocampal processing is not selective to any particular category of learning materials; instead, it supports comparisons among all kinds of information in memory, resulting in a representation of critical relations between items. Conversely, individual representations are supported outside the hippocampal system. Second, hippocampal-dependent, relational memory representations involve a flexible organization that permits inferences from memory in novel situations. Conversely, hippocampal-independent individual representations can support only repetition of procedures acquired during original learning. Correspondences between the neuropsychological and neurophysiological findings presented serve to indicate how these properties of hippocampal representation support declarative memory across behavioral paradigms and across species.

[1]  D. Kimble The effects of bilateral hippocampal lesions in rats. , 1963, Journal of comparative and physiological psychology.

[2]  D. Kimble,et al.  Olfactory discrimination in rats with hippocampal lesions , 1967 .

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

[5]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[6]  A. R. Lurii︠a︡,et al.  The neuropsychology of memory , 1977 .

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

[8]  James L Olds,et al.  Effects of context manipulation on memory and reversal learning in rats with hippocampal lesions. , 1978, Journal of comparative and physiological psychology.

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

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

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

[12]  P. Best,et al.  Spatial correlates of hippocampal unit activity are altered by lesions of the fornix and entorhinal cortex , 1980, Brain Research.

[13]  A. J. Hill,et al.  Effects of deafness and blindness on the spatial correlates of hippocampal unit activity in the rat , 1981, Experimental Neurology.

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

[15]  R. Morris Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

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

[17]  G. Lynch,et al.  Hippocampal denervation causes rapid forgetting of olfactory information in rats. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Daniel L. Schacter,et al.  Multiple forms of memory in humans and animals , 1985 .

[19]  H. Niki,et al.  Hippocampal unit activity and delayed response in the monkey , 1985, Brain Research.

[20]  L. Squire,et al.  Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. , 1985, Behavioral neuroscience.

[21]  Differential effects of posterior septal lesions on dispositional and representational memory. , 1986 .

[22]  J. N. P. Rawlins,et al.  Comparator and Buffer Memory , 1986 .

[23]  D. Olton,et al.  Mnemonic correlates of unit activity in the hippocampus , 1986, Brain Research.

[24]  Richard F. Thompson,et al.  Role of the Hippocampus in Classical Conditioning of Aversive and Appetitive Behaviors , 1986 .

[25]  M. Kuperstein,et al.  Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  L. Squire Memory and Brain , 1987 .

[27]  D. Schacter,et al.  The Evolution of Multiple Memory Systems , 1987 .

[28]  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.

[29]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  R. Hampson,et al.  Sequential dependencies regulate sensory evoked responses of single units in the rat hippocampus , 1987, Brain Research.

[31]  H. Eichenbaum,et al.  Representation in the hippocampus: what do hippocampal neurons code? , 1988, Trends in Neurosciences.

[32]  E. Halgren,et al.  Neural encoding of individual words and faces by the human hippocampus and amygdala , 1988, Nature.

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

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

[35]  R. J. McDonald,et al.  Damage to the hippocampal formation in rats selectively impairs the ability to learn cue relationships. , 1989, Behavioral and neural biology.

[36]  E. Rolls,et al.  Activity of hippocampal formation neurons in the monkey related to a conditional spatial response task. , 1989, Journal of neurophysiology.

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

[38]  H. Eichenbaum,et al.  Spatial and behavioral correlates of hippocampal neuronal activity , 1989 .

[39]  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.

[40]  Y. Miyashita,et al.  Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  Lawrence Weiskrantz,et al.  The effects of fornix transection and combined fornix transection, mammillary body lesions and hippocampal ablations on object-pair association memory in the rhesus monkey , 1989, Behavioural Brain Research.

[42]  Yoshio Sakurai,et al.  Hippocampal cells have behavioral correlates during the performance of an auditory working memory task in the rat , 1990 .

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

[44]  Y Sakurai,et al.  Hippocampal cells have behavioral correlates during the performance of an auditory working memory task in the rat. , 1990, Behavioral neuroscience.

[45]  L. Nadel The hippocampus and space revisited , 1991, Hippocampus.

[46]  Taketoshi Ono,et al.  Place recognition responses of neurons in monkey hippocampus , 1991, Neuroscience Letters.

[47]  H Eichenbaum,et al.  The theory that wouldn't die: A critical look at the spatial mapping theory of hippocampal function , 1991, Hippocampus.

[48]  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.

[49]  Howard Eichenbaum,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 .

[50]  H. Eichenbaum,et al.  Neuronal activity in the hippocampus during delayed non‐match to sample performance in rats: Evidence for hippocampal processing in recognition memory , 1992, Hippocampus.

[51]  Larry R. Squire,et al.  Neuropsychology of memory, 2nd ed. , 1992 .

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