Stress‐induced cortisol modulates the control of memory retrieval towards the dorsal striatum

Abstract

Stress can modulate the recruitment of multiple memory systems during learning, favouring dorsal striatal “habit” learning over hippocampal “cognitive” learning. Here, we tested whether stress may also bias the engagement of “cognitive” and “habit” systems during retrieval and thereby affect the nature of remembering. To this end, participants first performed a probabilistic classification learning task that can be solved by both the “cognitive” and the “habit” system. Twenty‐four hours later, participants underwent either a stress manipulation or a non‐stressful control procedure before they completed a retention test for the previously learned task in the MRI scanner. During this retention test, stress‐induced cortisol levels were linked to a relative bias towards behavioural strategies indicative for the “habit” system. At the neural level, stress led to increased dorsal striatal activity during retrieval. Elevated cortisol levels were directly correlated with increased activity in the dorsal striatum and further linked to reduced functional connectivity between the hippocampus and the amygdala, which is assumed to orchestrate the stress‐related shift from “cognitive” to “habitual” control. Together, our data suggest that stress may bias the contributions of multiple memory systems also at retrieval, in a manner that promotes dorsal striatal “habit” processes and most likely driven by cortisol.

Place vs. Response Learning: History, Controversy, and Neurobiology

“…The enhancing effect of corticosterone or RS 79948-197 on response learning may be blocked by concurrent infusion of anxiolytic drugs (Leong et al, 2012;Goodman et al, 2015). Importantly, the enhancement of response learning following stress/anxiety has not only been demonstrated in rats using plus-maze tasks (Packard and Wingard, 2004) but has also been observed using response learning or ''habit'' memory tasks designed for human subjects (Schwabe et al, 2007(Schwabe et al, , 2008(Schwabe et al, , 2013Schwabe andWolf, 2009, 2010;Guenzel et al, 2014;Goldfarb et al, 2017;Goodman et al, 2020;Zerbes et al, 2020).…”

Mental Resilience and Coping With Stress: A Comprehensive, Multi-level Model of Cognitive Processing, Decision Making, and Behavior

“…In other words, ''cold'' executive functioning is set to prioritize the most reliable decision-making to avoid danger when confronting a threat, yet it limits attention and flexibility. The mechanism is facilitated by promoted dorsal striatum-dependent (''habit'') learning and behavior over hippocampal-dependent (''cognitive'') memory encoding and retrieval, which leads to stereotypical ideas and thus maladaptive functioning in chronic stress (e.g., Packard, 2009;Vogel and Schwabe, 2016;Vogel et al, 2017;Zerbes et al, 2020; see also Schiebener and Brand, 2015;Shimp et al, 2015;Fitoussi et al, 2018). In particular, poor consequences can be seen in attentional set-shifting deficits, poor memory, anxiety, and depression (e.g., Palamarchuk and Vaillancourt, under review).…”

Integrative Brain Dynamics in Childhood Bullying Victimization: Cognitive and Emotional Convergence Associated With Stress Psychopathology

“…Under stress, the amygdala also promotes functional connectivity with the dorsal striatum that reduces its functional connectivity with the hippocampus, impacting the quantity and quality of memory; in particular, the established coupling shifts memory encoding and retrieval from hippocampus-dependent (“cognitive”) to striatum-dependent (“habit”) mode (Packard, 2009 ; Vogel and Schwabe, 2016 ; Vogel et al, 2017 ; Zerbes et al, 2020 ). The dorsal striatum relates to the automatic/habit responses and attention regulation via the PFC and parietal cortical interactions (e.g., Lago et al, 2017 ) and the implication of this shift is that the memory process reduces flexibility and thus becomes more reflexive.…”