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Parallel processing across neural systems: implications for a multiple memory system hypothesis.
Neurobiol Learn Mem. 2004 Nov; 82(3):278-98.NL

Abstract

A common conceptualization of the organization of memory systems in brain is that different types of memory are mediated by distinct neural systems. Strong support for this view comes from studies that show double (or triple) dissociations between spatial, response, and emotional memories following selective lesions of hippocampus, striatum, and the amygdala. Here, we examine the extent to which hippocampal and striatal neural activity patterns support the multiple memory systems view. A comparison is made between hippocampal and striatal neural correlates with behavior during asymptotic performance of spatial and response maze tasks. Location- (or place), movement, and reward-specific firing patterns were found in both structures regardless of the task demands. Many, but not all, place fields of hippocampal and striatal neurons were similarly affected by changes in the visual and reward context regardless of the cognitive demands. Also, many, but not all, hippocampal and striatal movement-sensitive neurons showed significant changes in their behavioral correlates after a change in visual context, irrespective of cognitive strategy. Similar partial reorganization was observed following manipulations of the reward condition for cells recorded from both structures, again regardless of task. Assuming that representations that persist across context changes reflect learned information, we make the following conclusions. First, the consistent pattern of partial reorganization supports a view that the analysis of spatial, response, and reinforcement information is accomplished via an error-driven, or match-mismatch, algorithm across neural systems. Second, task-relevant processing occurs continuously within hippocampus and striatum regardless of the cognitive demands of the task. Third, given the high degree of parallel processing across allegedly different memory systems, we propose that different neural systems may effectively compete for control of a behavioral expression system. The strength of the influence of any one neural system on behavioral output is likely modulated by factors such as motivation, experience, or hormone status.

Authors+Show Affiliations

Psychology Department, University of Washington, Box 351525, Seattle, WA 98155-1525, USA. mizumori@u.washington.eduNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.
Review

Language

eng

PubMed ID

15464410

Citation

Mizumori, Sheri J Y., et al. "Parallel Processing Across Neural Systems: Implications for a Multiple Memory System Hypothesis." Neurobiology of Learning and Memory, vol. 82, no. 3, 2004, pp. 278-98.
Mizumori SJ, Yeshenko O, Gill KM, et al. Parallel processing across neural systems: implications for a multiple memory system hypothesis. Neurobiol Learn Mem. 2004;82(3):278-98.
Mizumori, S. J., Yeshenko, O., Gill, K. M., & Davis, D. M. (2004). Parallel processing across neural systems: implications for a multiple memory system hypothesis. Neurobiology of Learning and Memory, 82(3), 278-98.
Mizumori SJ, et al. Parallel Processing Across Neural Systems: Implications for a Multiple Memory System Hypothesis. Neurobiol Learn Mem. 2004;82(3):278-98. PubMed PMID: 15464410.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Parallel processing across neural systems: implications for a multiple memory system hypothesis. AU - Mizumori,Sheri J Y, AU - Yeshenko,Oksana, AU - Gill,Kathryn M, AU - Davis,Denise M, PY - 2004/04/16/received PY - 2004/07/02/revised PY - 2004/07/12/accepted PY - 2004/10/7/pubmed PY - 2005/1/14/medline PY - 2004/10/7/entrez SP - 278 EP - 98 JF - Neurobiology of learning and memory JO - Neurobiol Learn Mem VL - 82 IS - 3 N2 - A common conceptualization of the organization of memory systems in brain is that different types of memory are mediated by distinct neural systems. Strong support for this view comes from studies that show double (or triple) dissociations between spatial, response, and emotional memories following selective lesions of hippocampus, striatum, and the amygdala. Here, we examine the extent to which hippocampal and striatal neural activity patterns support the multiple memory systems view. A comparison is made between hippocampal and striatal neural correlates with behavior during asymptotic performance of spatial and response maze tasks. Location- (or place), movement, and reward-specific firing patterns were found in both structures regardless of the task demands. Many, but not all, place fields of hippocampal and striatal neurons were similarly affected by changes in the visual and reward context regardless of the cognitive demands. Also, many, but not all, hippocampal and striatal movement-sensitive neurons showed significant changes in their behavioral correlates after a change in visual context, irrespective of cognitive strategy. Similar partial reorganization was observed following manipulations of the reward condition for cells recorded from both structures, again regardless of task. Assuming that representations that persist across context changes reflect learned information, we make the following conclusions. First, the consistent pattern of partial reorganization supports a view that the analysis of spatial, response, and reinforcement information is accomplished via an error-driven, or match-mismatch, algorithm across neural systems. Second, task-relevant processing occurs continuously within hippocampus and striatum regardless of the cognitive demands of the task. Third, given the high degree of parallel processing across allegedly different memory systems, we propose that different neural systems may effectively compete for control of a behavioral expression system. The strength of the influence of any one neural system on behavioral output is likely modulated by factors such as motivation, experience, or hormone status. SN - 1074-7427 UR - https://www.unboundmedicine.com/medline/citation/15464410/Parallel_processing_across_neural_systems:_implications_for_a_multiple_memory_system_hypothesis_ L2 - https://linkinghub.elsevier.com/retrieve/pii/S1074-7427(04)00080-2 DB - PRIME DP - Unbound Medicine ER -