Stress increases aversive prediction error signal in the ventral striatum

Abstract

From job interviews to the heat of battle, it is evident that people think and learn differently when stressed. In fact, learning under stress may have long-term consequences; stress facilitates aversive conditioning and associations learned during extreme stress may result in debilitating emotional responses in posttraumatic stress disorder. The mechanisms underpinning such stress-related associations, however, are unknown. Computational neuroscience has successfully characterized several mechanisms critical for associative learning under normative conditions. One such mechanism, the detection of a mismatch between expected and observed outcomes within the ventral striatum (i.e., "prediction errors"), is thought to be a critical precursor to the formation of new stimulusoutcome associations. An untested possibility, therefore, is that stress may affect learning via modulation of this mechanism. Here we combine a translational model of stress with a cognitive neuroimaging paradigm to demonstrate that stress significantly increases ventral striatum aversive (but not appetitive) prediction error signal. This provides a unique account of the propensity to form threat-related associations under stress with direct implications for our understanding of both normal stress and stress-related disorders.threat of shock | punishment | anxiety | face perception L earning to associate cues with threat is adaptive because it allows future threat to be predicted and avoided (1). However, such associative learning also may lead to haunting and debilitating memories; the smell of stir-fry may evoke painful intrusive memories in Vietnam veterans. How aversive information is integrated to guide adaptive or maladaptive behavior, however, is not well understood. Here, we report that stress increases a key learning mechanism: the neural detection of a mismatch between an expected and observed aversive outcome within the ventral striatum, commonly referred to as the aversive prediction error (PE) signal (1, 2).Neurocomputational and neuroeconomic accounts of cognition posit that stimulus-outcome associations during conditioning are formed via temporal difference learning (1, 3, 4), in which learning depends upon comparing expectation to what is currently happening. New associations, it is argued, are driven by a difference between predicted and actual outcomes (i.e., "prediction errors"), with greater mismatch between expected and actual outcomes evoking greater PE, resulting in greater predictive learning. This mismatch gives rise to phasic dopamine release in the ventral striatum (1, 3-5) for both appetitive and aversive stimuli (1, 2, 6, 7). Little is known, however, about how PE processing might be affected by an organism's emotional state. Stress, for instance, is well known to facilitate aversive conditioning in both humans and animals (8, 9), raising the possibility that aversive PEs also might be increased by stress. This hypothesis, however, is untested. Therefore, here we used a translational stress induction method in healt...

The impact of threat of shock-induced anxiety on memory encoding and retrieval

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“…The ventral portions of the caudate, including the accumbens, have traditionally been associated with transient, reward-related processes (Haber and Knutson, 2009), but recent more research has suggests a potential role for the nucleus accumbens during aversive processing (Becerra et al, 2001; Cabib and Puglisi-Allegra, 1994, 1996; Delgado et al, 2008; Jensen et al, 2003; McMenamin et al, 2014; Oleson et al, 2012; Robinson et al, 2013; Salamone, 1994; Schoenbaum and Setlow, 2003). Critically, this accumbens region of interest may have gone unnoticed if common data analysis strategies were used to search for connectivity changes (such as using amygdala-based seed analysis).…”

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