Normal olfactory discrimination learning set and facilitation of reversal learning after medial-temporal damage in rats: implications for an account of preserved learning abilities in amnesia

Recent evidence of preserved skill learning in patients with “global” amnesia has led to the postulation of a qualitative distinction between functionally separate memory systems, one of which may remain preserved when the other is profoundly impaired. On one account, the separate memory systems support either the learning of declarative knowledge, i.e., facts and associations, or the learning of procedural knowledge, i.e., knowledge that permits the expression of skilled performance without reference to specific facts or associations. In an effort to develop a rodent model of amnesia that illustrates the same distinction between memory systems, rats were trained in a series of discrimination and reversal problems using olfaction, a sensory modality in which they rapidly learn new associations. Rats with bilateral fornix, amygdala, or combined fornix and amygdala damage learned successive two-odor discriminations as quickly as normal and sham-operated control subjects. Furthermore, all groups rapidly acquired the skills of discrimination as revealed in the development of a learning set. Subsequent presentation of a reversal of one discrimination elicited a marked dissociation among groups: Normal rats and rats with amygdala lesions required many more trials to acquire the reversal than to acquire a new discrimination problem, whereas rats with fornix lesions learned the reversal rather easily. A detailed analysis of response strategies suggested that normal rats and rats with amygdala lesions first extinguished the prior response tendencies and then abandoned the learning set skills and treated the reversal much as they did the initial discrimination problem.(ABSTRACT TRUNCATED AT 250 WORDS)

[1]  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.

[2]  D. Kimble Hippocampus and internal inhibition. , 1968, Psychological bulletin.

[3]  Richard Hirsh,et al.  The hippocampus, conditional operations, and cognition , 1980 .

[4]  E. Warrington,et al.  Conditioning in amnesic patients , 1979, Neuropsychologia.

[5]  R. Douglas,et al.  The hippocampus and behavior. , 1967, Psychological bulletin.

[6]  H. Teitelbaum A COMPARISON OF EFFECTS OF ORBITOFRONTAL AND HIPPOCAMPAL LESIONS UPON DISCRIMINATION LEARNING AND REVERSAL IN THE CAT. , 1964, Experimental neurology.

[7]  John O'Keefe,et al.  On the trail of the hippocampal engram , 1980 .

[8]  H Eichenbaum,et al.  Thalamocortical mechanisms in odor-guided behavior. I. Effects of lesions of the mediodorsal thalamic nucleus and frontal cortex on olfactory discrimination in the rat. , 1980, Brain, behavior and evolution.

[9]  D. Webster,et al.  LEARNING DEFICITS FOLLOWING HIPPOCAMPAL LESIONS IN SPLIT-BRAIN CATS. , 1964, Experimental neurology.

[10]  S. Zola-Morgan,et al.  Hippocampal resections impair associative learning and recognition memory in the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  E. Greene,et al.  Behavioral role of hippocampal connections. , 1974, Experimental neurology.

[12]  R. Isaacson,et al.  Task dependent recovery after early brain damage. , 1973, Behavioral biology.

[13]  M. Moss,et al.  Consolidation of memory the hippocampus revisited , 1984 .

[14]  B. Slotnick,et al.  Olfactory Learning-Set Formation in Rats , 1974, Science.

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

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

[17]  E. Tulving How many memory systems are there , 1985 .

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

[19]  T. S. Brown,et al.  Hippocampal lesions and learned taste aversion , 1974 .

[20]  G. Winocur Effects of interference on discrimination learning and recall by rats with hippocampal lesions , 1979, Physiology & Behavior.

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

[22]  David S. Olton,et al.  A disconnection analysis of hippocampal function , 1982, Brain Research.

[23]  G. Handelmann,et al.  Hippocampal function: Working memory or cognitive mapping? , 1980 .

[24]  R. C. Tees,et al.  Optional intradimensional and extradimensional shifts in the rat. , 1971, Journal of comparative and physiological psychology.

[25]  Larry R. Squire,et al.  CHAPTER 6 – THE NEUROLOGY OF MEMORY: THE CASE FOR CORRESPONDENCE BETWEEN THE FINDINGS FOR HUMAN AND NONHUMAN PRIMATE1 , 1983 .

[26]  D. Olton,et al.  Object discrimination by rats: The role of frontal and hippocampal systems in retention and reversal , 1980, Physiology & Behavior.

[27]  L. Squire,et al.  Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  D. Kimble,et al.  Brightness discrimination and reversal in hippocampally-lesioned rats , 1968 .

[29]  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.

[30]  D. Gaffan,et al.  Monkeys' Recognition Memory for Complex Pictures and the Effect of Fornix Transection , 1977, The Quarterly journal of experimental psychology.

[31]  G. Winocur The hippocampus and cue utilization , 1980 .

[32]  M. Mishkin,et al.  Monkeys with combined amygdalo-hippocampal lesions succeed in object discrimination learning despite 24-hour intertrial intervals. , 1984, Behavioral neuroscience.

[33]  J. Jennings,et al.  Olfactory Learning Set in Two Varieties of Domestic Rat , 1969, Psychological reports.

[34]  H. Eichenbaum,et al.  Thalamocortical mechanisms in odor-guided behavior. II. Effects of lesions of the mediodorsal thalamic nucleus and frontal cortex on odor preferences and sexual behavior in the hamster. , 1980, Brain, behavior and evolution.

[35]  F RESTLE,et al.  Toward a quantitate description of learning set data. , 1958, Psychological review.

[36]  D L Schacter,et al.  Priming of Old and New Knowledge in Amnesic Patients and Normal Subjects a , 1985, Annals of the New York Academy of Sciences.

[37]  L. Weiskrantz Comparative aspects of studies of amnesia. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  S. Zola-Morgan,et al.  Concurrent discrimination learning of monkeys after hippocampal, entorhinal, or fornix lesions , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  S M Zola,et al.  Paradoxical facilitation of object reversal learning after transection of the fornix in monkeys. , 1973, Neuropsychologia.

[40]  L. Jarrard Selective hippocampal lesions and behavior , 1980 .

[41]  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.

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

[43]  B. Kaada,et al.  Locomotor, avoidance and maze behavior in rats with the dorsal fornix transected , 1975, Physiology & Behavior.

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

[45]  Gordon Winocur,et al.  Transfer between related and unrelated problems following hippocampal lesions in rats. , 1970 .

[46]  I. Samuels Hippocampal lesions in the rat: effects on spatial and visual habits. , 1972, Physiology & behavior.

[47]  I. Krechevsky Brain mechanisms and "hypotheses." , 1935 .

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

[49]  W. B. Orr,et al.  Role of the Hippocampus in Reversal Learning of the Rabbit Nictitating Membrane Response , 1982 .

[50]  L. Cermak Human memory and amnesia , 1982 .

[51]  N. Cohen Neuropsychological evidence for a distinction between procedural and declarative knowledge in human memory and amnesia , 1981 .

[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]  Howard Eichenbaum,et al.  Reexamination of functional subdivisions of the rodent prefrontal cortex , 1983, Experimental Neurology.

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