Altered reward learning and hippocampal connectivity following psychosocial stress

Kruse, Onno; Stalder, Tobias; Stark, Rudolf; Klucken, Tim

doi:10.1016/j.neuroimage.2017.12.076

Cited by 35 publications

(33 citation statements)

References 72 publications

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“…Furthermore, uncontrollable auditory stimuli can elevate stress responses (Arguelles, Ibeas, Ottone, & Chekherdemian, 1962;Breier et al, 1987;Rylander, 2004;Westman & Walters, 1981) and may disrupt dopaminergic mechanisms (Arnsten et al, 1998) and cognitive functioning (Glass, Reim, & Singer, 1971). Whereas in studies using other well-validated stress manipulations, such as the cold pressor task (e.g., Byrne, Cornwall, & Worthy, 2019;Lighthall et al, 2013) or the Trier social test (e.g., Kruse, Tapia León, Stalder, Stark, & Klucken, 2018;Petzold et al, 2010), stress induction precedes task-solving (hence, learning), in our study we ensured that the stress induction occurred throughout the task, i.e. concurrently with learning.…”

Section: Introductionmentioning

confidence: 99%

Acute stress impairs reward learning in men

Carvalheiro

Conceição

Mesquita

et al. 2020

Preprint

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Acute stress is ubiquitous in everyday life, but the extent to which acute stress affects how people learn from the outcomes of their choices is still poorly understood. Here, we investigate how acute stress impacts reward and punishment learning in men using a reinforcement-learning task. Sixty-two male participants performed the task whilst under stress and control conditions. We observed that acute stress impaired participants' choice performance towards monetary gains, but not losses. To unravel the mechanism(s) underlying such impairment, we fitted a reinforcement-learning model to participants' trial-by-trial choices. Computational modeling indicated that under acute stress participants learned more slowly from positive prediction errors - when the outcomes were better than expected - consistent with stress-induced dopamine disruptions. Such mechanistic understanding of how acute stress impairs reward learning is particularly important given the pervasiveness of stress in our daily life and the impact that stress can have on our wellbeing and mental health.

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Section: Introductionmentioning

confidence: 99%

Acute stress impairs reward learning in men

Carvalheiro

Conceição

Mesquita

et al. 2020

Preprint

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“…Higher in‐group variance in the sample of the present sample might have decreased the power to detect these effects more than the increased sample size increased power. Second, the previous study applied a more strict protocol, only collecting data in the afternoon to have constant baseline cortisol levels for a secondary research question (Kruse et al, ). As this is known to affect emotional learning, it is possible, that variation in involvement of vACC and caudate nucleus during early extinction is moderated by the time of day, for example, due to variation in baseline cortisol levels (Merz, Stark, Vaitl, Tabbert, & Wolf, ).…”

Section: Discussionmentioning

confidence: 99%

“…Subjects were not instructed about the explicit CS‐UCS contingencies. The first trials of the CS+ and the CS− were later excluded from the analyses because learning could not have taken place yet (Kruse, Tapia León, Stalder, Stark, & Klucken, ). In each trial, a CS+ or CS− (blue or yellow rectangle) was presented for 6 s, followed by a fixation cross for a variable (1–3 s) interstimulus interval.…”

Section: Methodsmentioning

confidence: 99%

“…CS regressors were split into an early (CS+ early /CS− early ) and a late phase (CS+ late /CS− late ) to enable clear differentiation between early and late effects (Kruse et al, ; Kruse et al, ; LaBar, Gatenby, Gore, LeDoux, & Phelps, ). Events were modeled as stick functions and were convolved with the canonical hemodynamic response function.…”

Section: Methodsmentioning

confidence: 99%

“…For extinction training, the regressors were similar to acquisition, excluding the UCS+ because the CS+ was no longer reinforced and not modeling the first CS separately. CS regressors were split into an early (CS+ early /CS− early ) and a late phase (CS+ late /CS− late ) to enable clear differentiation between early and late effects (Kruse et al, 2017;Kruse et al, 2018;LaBar, Gatenby, Gore, LeDoux, & Phelps, 1998). Events were modeled as stick func-…”

Section: Functional Magnetic Resonance Imagingmentioning

confidence: 99%

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Amygdala and nucleus accumbens involvement in appetitive extinction

Kruse

Stark

Klucken

2020

Human Brain Mapping

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Extinction of appetitive conditioning is regarded as an important model for the treatment of psychiatric disorders like addiction. However, very few studies have investigated its neural correlates. Therefore, we investigated neural correlates of appetitive extinction in a large human sample including all genders (N = 76, 40 females) to replicate and extend results from a previous study. During differential appetitive conditioning, one stimulus (CS+) was paired with the chance to win a monetary reward, whereas another stimulus (CS−) was not. During appetitive extinction on the next day, neither the CS+ nor the CS− were reinforced. After successful acquisition of appetitive conditioning, the extinction phase elicited significant reductions of valence and arousal ratings toward the CS+ and a significant reduction in skin conductance responses to the CS+ from early to late extinction. On a neural level, early extinction showed significant differential (CS+ − CS−) activation in dACC and hippocampus, whereas involvement of the vACC and caudate nucleus did not replicate. The differential activation of amygdala and nucleus accumbens during late extinction was replicated, with the amygdala displaying significantly higher differential activation during the late phase of extinction as compared to the early phase of extinction. We show discernible signals for reward learning and extinction in subregions of amygdala and nucleus accumbens after extinction learning. This successful replication underlines the role of nucleus accumbens and amygdala in neural models of appetitive extinction in humans that was previously only based on animal findings.

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Appetitive conditioning with pornographic stimuli elicits stronger activation in reward regions than monetary and gaming‐related stimuli

Krikova,

Klein,

Kampa

et al. 2024

Human Brain Mapping

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Appetitive conditioning plays an important role in the development and maintenance of pornography‐use and gaming disorders. It is assumed that primary and secondary reinforcers are involved in these processes. Despite the common use of pornography and gaming in the general population appetitive conditioning processes in this context are still not well studied. This study aims to compare appetitive conditioning processes using primary (pornographic) and secondary (monetary and gaming‐related) rewards as unconditioned stimuli (UCS) in the general population. Additionally, it investigates the conditioning processes with gaming‐related stimuli as this type of UCS was not used in previous studies. Thirty‐one subjects participated in a differential conditioning procedure in which four geometric symbols were paired with either pornographic, monetary, or gaming‐related rewards or with nothing to become conditioned stimuli (CS + porn, CS + game, CS + money, and CS−) in an functional magnetic resonance imaging study. We observed elevated arousal and valence ratings as well as skin conductance responses for each CS+ condition compared to the CS−. On the neural level, we found activations during the presentation of the CS + porn in the bilateral nucleus accumbens, right medial orbitofrontal cortex, and the right ventral anterior cingulate cortex compared to the CS−, but no significant activations during CS + money and CS + game compared to the CS−. These results indicate that different processes emerge depending on whether primary and secondary rewards are presented separately or together in the same experimental paradigm. Additionally, monetary and gaming‐related stimuli seem to have a lower appetitive value than pornographic rewards.

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Altered reward learning and hippocampal connectivity following psychosocial stress

Cited by 35 publications

References 72 publications

Acute stress impairs reward learning in men

Acute stress impairs reward learning in men

Amygdala and nucleus accumbens involvement in appetitive extinction

Appetitive conditioning with pornographic stimuli elicits stronger activation in reward regions than monetary and gaming‐related stimuli

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