Multiple Memory Subsystems: Reconsidering Memory in the Mind and Brain

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.

Perceptual Generalization of Alcohol-Related Value Characterizes Risky Drinkers

“…This is consistent with findings in the fear domain, as forming more general Pavlovian threat associations was also associated with lower episodic memory specificity (Starita et al, 2019), and lower episodic pattern separation was also associated with broader threat generalization (Lange et al, 2017). More work is needed to understand the mechanisms linking these two memory systems Sherman et al, 2023) and how they may be modulated by alcohol history.…”

Acute stress effects on statistical learning and episodic memory

“…In the absence of stress, there was a negative association between episodic memory (hit rate) and offline statistical learning (pair familiarity). This finding is consistent with the idea that their shared reliance on the hippocampus and output pathways may create interference (Schapiro et al, 2017;Sučević and Schapiro, 2023;Sherman et al, 2023b). However, the relationship between these memory metrics under stress was more nuanced, varying with time since stress and with the predictable nature of the memoranda.…”

“…Multiple frameworks have sought to explain these deleterious effects of stress on memory via its detrimental effects on the hippocampus (e.g., Diamond et al 2007;Lupien et al 2007; Goldfarb and Phelps 2017; Schwabe et al 2022; but see Goldfarb 2019). However, these theories ignore a critical feature of hippocampal function: the hippocampus is not a homogeneous structure dedicated to episodic memory (Henke, 2010;Shohamy and Turk-Browne, 2013;Duncan and Schlichting, 2018;Sherman et al, 2023b). Instead, the hippocampus also supports a distinct mnemonic process of statistical learning.…”

A neural network model of hippocampal contributions to category learning

“…In a recent paper, we adopted a version of C-HORSE that invoked such a control function in order to explain behavior across tasks with different demands in an associative inference paradigm ( Zhou et al, 2023 ). Medial prefrontal cortex could potentially carry out a control function of this kind ( Sherman et al, 2023 ), as it participates in category learning ( Mack et al, 2020 ) and is known to modulate CA1 representations as a function of task ( Eichenbaum, 2017 ; Guise and Shapiro, 2017 ). As the TSP and MSP are both routed through CA1, medial prefrontal control over CA1 could conceivably help coordinate information flow there for optimal behavior.…”