Variants of olfactory memory and their dependencies on the hippocampal formation

Olfactory memory in control rats and in animals with entorhinal cortex lesions was tested in four paradigms: (1) a known correct odor was present in a group of familiar but nonrewarded odors, (2) six known correct odors were simultaneously present in a maze, (3) correct responses required the learning of associations between odors and objects, and (4) six odors, each associated with a choice between two objects, were presented simultaneously. Control rats had no difficulty with the first problem and avoided repeating selections in the second; this latter behavior resembles that reported for spatial mazes but, in the present experiments, was not dependent upon memory for the configuration of pertinent cues. Control animals varied considerably in their acquisition of odor-object associations with only a subgroup learning every set of pairings. These latter animals also performed well in the fourth task and, as indicated by post hoc analyses, developed complex strategies in dealing with the problem of serial odor- object pairs. Lesioned animals had no difficulty in selecting correct odors learned prior to surgery (problem one) but repeated their choices in problem two. This latter result suggests that hippocampus contributes to the transient memory of prior choices for odors as it does for prior choices in spatial mazes. Entorhinal rats were able to form odor-object associations (problem three), and a subgroup of the animals periodically succeeded in doing a long series of such choices (problem four), though with less frequency than controls. These results indicate that rats use both long-term memory and transient memory in dealing with olfactory problems and suggest that the second of these is dependent upon a hippocampal process that encodes a type of information other than the relationship between cues.

[1]  J. Besson,et al.  The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: A phaseolus vulgaris leucoagglutinin (PHA‐L) study in the rat , 1993, The Journal of comparative neurology.

[2]  O. Ottersen,et al.  Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase , 1982, The Journal of comparative neurology.

[3]  O. Steward,et al.  On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. , 1984, Behavioral neuroscience.

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

[5]  L. Haberly,et al.  NMDA-dependent induction of long-term potentiation in afferent and association fiber systems of piriform cortex in vitro , 1990, Brain Research.

[6]  G. Lynch,et al.  Antagonism of NMDA receptors impairs acquisition but not retention of olfactory memory. , 1989, Behavioral neuroscience.

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

[8]  A. Hjorth-Simonsen,et al.  Projection of the lateral part of the entorhinal area to the hippocampus and fascia dentata , 1972, The Journal of comparative neurology.

[9]  H. Groenewegen,et al.  Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid , 1980, Neuroscience.

[10]  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.

[11]  G. Lynch,et al.  Synaptic rearrangement in the dentate gyrus: histochemical evidence of adjustments after lesions in immature and adult rats. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Lynch,et al.  Induced acetylcholinesterase-rich layer in rat dentate gyrus following entorhinal lesions. , 1972, Brain research.

[13]  R. Nicoll,et al.  Mossy fiber long-term potentiation shows specificity but no apparent cooperativity , 1992, Neuroscience Letters.

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

[15]  Gary Lynch,et al.  Stable depression of potentiated synaptic responses in the hippocampus with 1–5 Hz stimulation , 1990, Brain Research.

[16]  J Larson,et al.  Mossy fiber potentiation and long‐term potentiation involve different expression mechanisms , 1990, Synapse.

[17]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[18]  David E. Hornung,et al.  A method for establishing a five odorant identification confusion matrix task in rats , 1990, Physiology & Behavior.

[19]  H. Eichenbaum,et al.  Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  G Lynch,et al.  Facilitation of glutamate receptors enhances memory. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. II. Hippocampal slow waves and theta cell firing during bar pressing and other behaviors. , 1973, Experimental neurology.

[22]  A peculiar form of potentiation in mossy fiber synapses. , 1992, Epilepsy research. Supplement.

[23]  E. Lauterbach The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1993 .

[24]  H. Groenewegen,et al.  The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. , 1990, Progress in brain research.

[25]  G. Lynch,et al.  Olfaction and the "data" memory system in rats. , 1987, Behavioral neuroscience.

[26]  G. Lynch,et al.  Evidence for synaptic potentiation in a cortical network during learning , 1987, Brain Research.

[27]  M. Witter Organization of the entorhinal—hippocampal system: A review of current anatomical data , 1993, Hippocampus.

[28]  G Lynch,et al.  Studies on retrograde and anterograde amnesia of olfactory memory after denervation of the hippocampus by entorhinal cortex lesions. , 1986, Behavioral and neural biology.

[29]  L. Heimer The Olfactory Cortex and the Ventral Striatum , 1978 .

[30]  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.

[31]  G. Lynch,et al.  Stable hippocampal long-term potentiation elicited by ‘theta’ pattern stimulation , 1987, Brain Research.

[32]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. , 1992, Behavioral neuroscience.

[33]  H. Nauta A proposed conceptual reorganization of the basal ganglia and telencephalon , 1979, Neuroscience.

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

[35]  Bruce L. McNaughton,et al.  A systematic test of cognitive mapping, working-memory, and temporal discontiguity theories of hippocampal function , 1989, Psychobiology.

[36]  H. Eichenbaum,et al.  Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task , 1992 .

[37]  D. Olton,et al.  Hippocampal and amygdaloid involvement in working memory for nonspatial stimuli. , 1988, Behavioral neuroscience.

[38]  W. Nauta,et al.  An intricately patterned prefronto‐caudate projection in the rhesus monkey , 1977, The Journal of comparative neurology.