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      Multiple Memory Subsystems: Reconsidering Memory in the Mind and Brain

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          Abstract

          The multiple-memory-systems framework—that distinct types of memory are supported by distinct brain systems—has guided learning and memory research for decades. However, recent work challenges the one-to-one mapping between brain structures and memory types central to this taxonomy, with key memory-related structures supporting multiple functions across substructures. Here we integrate cross-species findings in the hippocampus, striatum, and amygdala to propose an updated framework of multiple memory subsystems (MMSS). We provide evidence for two organizational principles of the MMSS theory: First, opposing memory representations are colocated in the same brain structures; second, parallel memory representations are supported by distinct structures. We discuss why this burgeoning framework has the potential to provide a useful revision of classic theories of long-term memory, what evidence is needed to further validate the framework, and how this novel perspective on memory organization may guide future research.

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          Most cited references192

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          Cognitive maps in rats and men.

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            Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action.

            Recent behavioral studies in both humans and rodents have found evidence that performance in decision-making tasks depends on two different learning processes; one encoding the relationship between actions and their consequences and a second involving the formation of stimulus-response associations. These learning processes are thought to govern goal-directed and habitual actions, respectively, and have been found to depend on homologous corticostriatal networks in these species. Thus, recent research using comparable behavioral tasks in both humans and rats has implicated homologous regions of cortex (medial prefrontal cortex/medial orbital cortex in humans and prelimbic cortex in rats) and of dorsal striatum (anterior caudate in humans and dorsomedial striatum in rats) in goal-directed action and in the control of habitual actions (posterior lateral putamen in humans and dorsolateral striatum in rats). These learning processes have been argued to be antagonistic or competing because their control over performance appears to be all or none. Nevertheless, evidence has started to accumulate suggesting that they may at times compete and at others cooperate in the selection and subsequent evaluation of actions necessary for normal choice performance. It appears likely that cooperation or competition between these sources of action control depends not only on local interactions in dorsal striatum but also on the cortico-basal ganglia network within which the striatum is embedded and that mediates the integration of learning with basic motivational and emotional processes. The neural basis of the integration of learning and motivation in choice and decision-making is still controversial and we review some recent hypotheses relating to this issue.
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              Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory.

              Damage to the hippocampal system disrupts recent memory but leaves remote memory intact. The account presented here suggests that memories are first stored via synaptic changes in the hippocampal system, that these changes support reinstatement of recent memories in the neocortex, that neocortical synapses change a little on each reinstatement, and that remote memory is based on accumulated neocortical changes. Models that learn via changes to connections help explain this organization. These models discover the structure in ensembles of items if learning of each item is gradual and interleaved with learning about other items. This suggests that the neocortex learns slowly to discover the structure in ensembles of experiences. The hippocampal system permits rapid learning of new items without disrupting this structure, and reinstatement of new memories interleaves them with others to integrate them into structured neocortical memory systems.
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                Author and article information

                Journal
                Perspect Psychol Sci
                Perspect Psychol Sci
                PPS
                sppps
                Perspectives on Psychological Science
                SAGE Publications (Sage CA: Los Angeles, CA )
                1745-6916
                1745-6924
                30 June 2023
                January 2024
                : 19
                : 1
                : 103-125
                Affiliations
                [1 ]Department of Psychology, University of Pennsylvania
                [2 ]Department of Psychology, Yale University
                [3 ]Wu Tsai Institute, Yale University
                [4 ]Department of Psychiatry, Yale University
                [5 ]National Center for PTSD, West Haven, USA
                Author notes
                [*]Brynn Sherman, Department of Psychology, University of Pennsylvania Email: brynns@ 123456sas.upenn.edu
                [*]Elizabeth Goldfarb, Department of Psychology, Yale University Email: elizabeth.goldfarb@ 123456yale.edu
                Author information
                https://orcid.org/0000-0002-5071-7101
                https://orcid.org/0000-0001-7519-3001
                Article
                10.1177_17456916231179146
                10.1177/17456916231179146
                10756937
                37390333
                e6cadc3f-9e1a-4033-9f32-4b07c4238e6f
                © The Author(s) 2023

                This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License ( https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

                History
                Funding
                Funded by: National Institute on Alcohol Abuse and Alcoholism, FundRef https://doi.org/10.13039/100000027;
                Award ID: K01 AA027832
                Funded by: Canadian Institute for Advanced Research, FundRef https://doi.org/10.13039/100007631;
                Funded by: National Institute of Mental Health, FundRef https://doi.org/10.13039/100000025;
                Award ID: R01 MH069456
                Funded by: National Institute of Mental Health, FundRef https://doi.org/10.13039/100000025;
                Award ID: R21 MH128740
                Funded by: National Science Foundation, FundRef https://doi.org/10.13039/100000001;
                Award ID: GRFP
                Categories
                Research Articles
                Custom metadata
                ts1

                hippocampus,striatum,amygdala,episodic memory,habits,conditioning

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