Corticosteroids Operate as a Switch between Memory Systems

Stress and corticosteroid hormones are known to affect learning and memory processes. In this study, we examined whether stress and corticosteroids are capable of facilitating the switch between multiple memory systems in mice. For this purpose, we designed a task that allowed measurement of nucleus caudate-based stimulus–response and hippocampus-based spatial learning strategies. Naive mice used spatial strategies to locate an exit hole on a circular hole board at a fixed location flagged by a proximal stimulus. When the mice were either stressed or administered corticosterone before the task, 30–50% of the mice switched to a stimulus–response strategy. This switch between learning strategies was accompanied by a rescue of performance, whereas performance declined in the stressed mice that kept using the spatial strategy. Pretreatment with a mineralocorticoid receptor antagonist prevented the switch toward the stimulus–response strategy but led to deterioration of hippocampus-dependent performance. These findings (i) show that corticosteroids promote the transition from spatial to stimulus–response memory systems, (ii) provide evidence that the mineralocorticoid receptor underlies this corticosteroid-mediated switch, and (iii) suggest that a stress-induced switch from hippocampus-based to nucleus caudate-based memory systems can rescue performance.

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Running Promotes Spatial Bias Independently of Adult Neurogenesis

10.1101/125260 ◽

2017 ◽

Author(s):

Jason S. Snyder ◽

Shaina P. Cahill ◽

Paul W. Frankland

Keyword(s):

Adult Neurogenesis ◽

Dorsal Striatum ◽

Memory Systems ◽

Hippocampal Neurogenesis ◽

Adult Hippocampal Neurogenesis ◽

Response Strategy ◽

Response Strategies ◽

Spatial Strategies ◽

Conflict Situations ◽

Exercise Induced

ABSTRACTDifferent memory systems offer distinct advantages to navigational behavior. The hippocampus forms complex associations between environmental stimuli, enabling flexible navigation through space. In contrast, the dorsal striatum associates discrete cues and favorable behavioral responses, enabling habit-like, automated navigation. While these two systems often complement one another, there are instances where striatal-dependent responses (e.g. approach a cue) conflict with hippocampal representations of spatial goals. In conflict situations, preference for spatial vs. response strategies varies across individuals and depends on previous experience, plasticity and the integrity of these two memory systems. Here, we investigated the role of adult hippocampal neurogenesis and exercise on mouse search strategies in a water maze task that can be solved with either a hippocampal-dependent place strategy or a striatal-dependent cue-response strategy. We predicted that inhibiting adult neurogenesis would impair hippocampal function and shift behavior towards striatal-dependent cue responses. However, blocking neurogenesis in a transgenic nestin-TK mouse did not affect strategy choice. We then investigated whether a pro-neurogenic stimulus, running, would bias mice towards hippocampal-dependent spatial strategies. While running indeed promoted spatial strategies, it did so even when neurogenesis was inhibited in nestin-TK mice. These findings indicate that exercise-induced increases in neurogenesis are not always required for enhanced cognitive function. Furthermore, our data identify exercise as a potentially useful strategy for promoting flexible, cognitive forms of memory in habit-related disorders that are characterized by excessive responding to discrete cues.

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Acute Stress Time-dependently Modulates Multiple Memory Systems

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01167 ◽

2017 ◽

Vol 29 (11) ◽

pp. 1877-1894 ◽

Cited By ~ 12

Author(s):

Elizabeth V. Goldfarb ◽

Yeva Mendelevich ◽

Elizabeth A. Phelps

Keyword(s):

Individual Differences ◽

Acute Stress ◽

Memory Systems ◽

Cognitive Mechanisms ◽

Cortisol Reactivity ◽

Preferential Expression ◽

Multiple Memory Systems ◽

Stimulus Response ◽

Adrenergic Activity ◽

Context Memory

Acute stress has been shown to modulate the engagement of different memory systems, leading to preferential expression of stimulus–response (SR) rather than episodic context memory when both types of memory can be used. However, questions remain regarding the cognitive mechanism that underlies this bias in humans—specifically, how each form of memory is individually influenced by stress in order for SR memory to be dominant. Here we separately measured context and SR memory and investigated how each was influenced by acute stress after learning (Experiment 1) and before retrieval (Experiment 2). We found that postlearning stress, in tandem with increased adrenergic activity during learning, impaired consolidation of context memory and led to preferential expression of SR rather than context memory. Preretrieval stress also impaired context memory, albeit transiently. Neither postlearning nor preretrieval stress changed the expression of SR memory. However, individual differences in cortisol reactivity immediately after learning were associated with variability in initial SR learning. These results reveal novel cognitive mechanisms by which stress can modulate multiple memory systems.

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Multiple memory systems

10.1093/oso/9780198824091.003.0004 ◽

2018 ◽

Author(s):

Richard J. Beninger

Keyword(s):

Declarative Memory ◽

Dorsal Striatum ◽

Recognition Task ◽

Memory Systems ◽

Learning Task ◽

Hippocampal Damage ◽

Incentive Learning ◽

Multiple Memory Systems ◽

Stimulus Response ◽

Memory Rats

Multiple memory systems describes how memories can be declarative or non-declarative; incentive learning produces one type of non-declarative memory. Patients with bilateral hippocampal damage have declarative memory deficits (amnesia) but intact non-declarative memory; patients with striatal dysfunction, for example, Parkinson’s patients who lose striatal dopamine have impaired incentive learning but intact declarative memory. Rats with lesions of the fornix (hippocampal output pathway), but not lesions of the dorsal striatum, have impaired spatial (declarative) memory; rats with lesions of the dorsal striatum, but not fornix, have impaired stimulus–response memory that relies heavily on incentive learning. These memory systems possibly inhibit one another to control responding: in rats, a group that received fornix lesions and had impaired spatial learning did better on an incentive task; in humans, hippocampus damage was associated with improvement on an incentive learning task and striatal damage was associated with increased involvement of the hippocampus in a route-recognition task.

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Mineralocorticoid Receptor Blockade Prevents Stress-Induced Modulation of Multiple Memory Systems in the Human Brain

Biological Psychiatry ◽

10.1016/j.biopsych.2013.06.001 ◽

2013 ◽

Vol 74 (11) ◽

pp. 801-808 ◽

Cited By ~ 101

Author(s):

Lars Schwabe ◽

Martin Tegenthoff ◽

Oliver Höffken ◽

Oliver T. Wolf

Keyword(s):

Human Brain ◽

Mineralocorticoid Receptor ◽

Memory Systems ◽

Receptor Blockade ◽

Multiple Memory Systems ◽

Mineralocorticoid Receptor Blockade

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Faculty Opinions recommendation of Mineralocorticoid receptor blockade prevents stress-induced modulation of multiple memory systems in the human brain.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718043515.793489888 ◽

2014 ◽

Author(s):

E Ronald de Kloet ◽

Onno Meijer

Keyword(s):

Human Brain ◽

Mineralocorticoid Receptor ◽

Memory Systems ◽

Receptor Blockade ◽

Multiple Memory Systems ◽

Mineralocorticoid Receptor Blockade

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Model-Based and Model-Free Social Cognition

10.31234/osf.io/ue6j2 ◽

2019 ◽

Author(s):

Leor M Hackel ◽

Jeffrey Jordan Berg ◽

Björn Lindström ◽

David Amodio

Keyword(s):

Reinforcement Learning ◽

Social Cognition ◽

Learning Strategies ◽

Memory Systems ◽

Learning Task ◽

Financial Advisors ◽

Model Based ◽

Model Free ◽

Systems Model ◽

Task Assessment

Do habits play a role in our social impressions? To investigate the contribution of habits to the formation of social attitudes, we examined the roles of model-free and model-based reinforcement learning in social interactions—computations linked in past work to habit and planning, respectively. Participants in this study learned about novel individuals in a sequential reinforcement learning paradigm, choosing financial advisors who led them to high- or low-paying stocks. Results indicated that participants relied on both model-based and model-free learning, such that each independently predicted choice during the learning task and self-reported liking in a post-task assessment. Specifically, participants liked advisors who could provide large future rewards as well as advisors who had provided them with large rewards in the past. Moreover, participants varied in their use of model-based and model-free learning strategies, and this individual difference influenced the way in which learning related to self-reported attitudes: among participants who relied more on model-free learning, model-free social learning related more to post-task attitudes. We discuss implications for attitudes, trait impressions, and social behavior, as well as the role of habits in a memory systems model of social cognition.

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