Hippocampal context processing is critical for interference free recall of odor memories in rats

Interference is a critical problem for memory systems and a primary cause of retrieval failure. One strategy for minimizing interference is to associate the items to be remembered with the context in which they were learned. For example, human subjects who learn two lists of words in separate contexts experience less interference and better recall than subjects who learn both lists in the same context. The hippocampus has long been known to be involved in processing contextual information and recent studies have shown that hippocampal neurons exhibit context‐unique firing patterns that could serve as a neural representation of the context. These observations suggest that hippocampal context processing may play a critical role in overcoming interference. To test this hypothesis, we adapted the context based list learning procedure for use with rats. Control rats and rats given temporary lesions of the hippocampus were trained on two lists of eight odor pairs, either in the same context or in different contexts. To induce interference, some of the odors appeared on both lists with their predictive value reversed. As with human subjects, rats that learned the two lists in different contexts performed significantly better than rats that learned the lists in the same context. However, hippocampal lesions completely abolished this contextual learning advantage. We also trained rats on a low interference version of the task by using lists that did not contain any common items. Interestingly, rats with hippocampal lesions were entirely unimpaired when the learning situation did not involve high levels of interference. These findings are consistent with the idea that the hippocampus encodes contexts and further suggest that hippocampal context coding is beneficial because it provides a means of overcoming interference. © 2011 Wiley‐Liss, Inc.

[1]  A. Baddeley,et al.  Context-dependent memory in two natural environments: on land and underwater. , 1975 .

[2]  H. Eichenbaum,et al.  The hippocampus and memory for orderly stimulus relations. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Steven M. Smith Environmental context—dependent memory. , 1988 .

[4]  David S. Olton,et al.  Hippocampal function and interference , 1994 .

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

[6]  David M. Smith,et al.  Hippocampal episode fields develop with learning , 2011, Hippocampus.

[7]  G. Davies,et al.  Memory in context : context in memory , 1990 .

[8]  M. Eacott,et al.  Behavioral / Systems / Cognitive Integrated Memory for Object , Place , and Context in Rats : A Possible Model of Episodic-Like Memory ? , 2004 .

[9]  H Eichenbaum,et al.  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 , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[11]  S J Mizumori,et al.  Hippocampal Representational Organization and Spatial Context , 1999, Hippocampus.

[12]  Matthew L. Shapiro,et al.  Motivational states activate distinct hippocampal representations to guide goal-directed behaviors , 2009, Proceedings of the National Academy of Sciences.

[13]  Thomas A Cleland,et al.  Behavioral models of odor similarity. , 2002, Behavioral neuroscience.

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

[15]  H. Eichenbaum,et al.  The Hippocampus and Disambiguation of Overlapping Sequences , 2002, The Journal of Neuroscience.

[16]  Howard Eichenbauma Using Olfaction to Study Memory , 1998 .

[17]  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.

[18]  M. Gabriel,et al.  Lesions of the entorhinal cortex disrupt behavioral and neuronal responses to context change during extinction of discriminative avoidance behavior , 1997, Experimental Brain Research.

[19]  Stephen Maren,et al.  Muscimol Inactivation of the Dorsal Hippocampus Impairs Contextual Retrieval of Fear Memory , 1999, The Journal of Neuroscience.

[20]  R. L. Gregory The Oxford companion to the mind , 1989 .

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

[22]  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.

[23]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[24]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

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

[26]  H Eichenbaum,et al.  The hippocampus and transverse patterning guided by olfactory cues. , 1998, Behavioral neuroscience.

[27]  Howard Eichenbaum,et al.  The Role of CA3 Hippocampal NMDA Receptors in Paired Associate Learning , 2006, The Journal of Neuroscience.

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

[29]  David M. Smith Provided for Non-commercial Research and Educational Use Only. Not for Reproduction, Distribution or Commercial Use. the Hippocampus, Context Processing and Episodic Memory , 2022 .

[30]  Paul E. Gilbert,et al.  Recognition memory for complex visual discriminations is influenced by stimulus interference in rodents with perirhinal cortex damage. , 2003, Learning & memory.

[31]  James L. McClelland,et al.  Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade‐off , 1994, Hippocampus.

[32]  M. Moser,et al.  Understanding memory through hippocampal remapping , 2008, Trends in Neurosciences.

[33]  David M. Smith,et al.  Fornix lesions impair context-related cingulothalamic neuronal patterns and concurrent discrimination learning in rabbits (Oryctolagus cuniculus). , 2004, Behavioral neuroscience.

[34]  H SCHLOSBERG,et al.  Similarity in stimulating conditions as a variable in retroactive inhibition. , 1951, Journal of experimental psychology.

[35]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[36]  Steven M. Smith,et al.  Environmental context-dependent memory: A review and meta-analysis , 2001, Psychonomic bulletin & review.

[37]  R. C. Honey,et al.  Context- but not familiarity-dependent forms of object recognition are impaired following excitotoxic hippocampal lesions in rats. , 2007, Behavioral neuroscience.

[38]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[39]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[40]  L. Jarrard What does the hippocampus really do? , 1995, Behavioural Brain Research.

[41]  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.

[42]  David M. Smith,et al.  Hippocampal place cells, context, and episodic memory , 2006, Hippocampus.

[43]  W E Skaggs,et al.  Interactions between location and task affect the spatial and directional firing of hippocampal neurons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  H Eichenbaum,et al.  Using olfaction to study memory. , 1998, Annals of the New York Academy of Sciences.

[45]  Oxana Eschenko,et al.  Non-commercial Research and Educational Use including without Limitation Use in Instruction at Your Institution, Sending It to Specific Colleagues That You Know, and Providing a Copy to Your Institution's Administrator. All Other Uses, Reproduction and Distribution, including without Limitation Comm , 2022 .

[46]  Greg D. Gale,et al.  Hippocampus and contextual fear conditioning: Recent controversies and advances , 2001, Hippocampus.

[47]  Jason D. Warren,et al.  The Oxford Companion to the Mind , 2005 .

[48]  David M. Smith,et al.  Learning-Related Development of Context-Specific Neuronal Responses to Places and Events: The Hippocampal Role in Context Processing , 2006, The Journal of Neuroscience.

[49]  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.