Stress effects on the neural substrates of motivated behavior

Hollon, Nick G.; Burgeno, Lauren M.; Phillips, Paul E. M.

doi:10.1038/nn.4114

Cited by 106 publications

(87 citation statements)

References 99 publications

(63 reference statements)

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“…Stress exposure can initiate a neuroendocrine cascade that modulates how individuals perceive and respond to rewarding or threatening cues in their environment (4–11). Specifically, it has been shown that stress may reduce acquisition of reward-related information (8, 12, 13) as well as disrupt normal reinforcer devaluation (9, 14, 15), two phenomena that are commonly observed in stress-related psychiatric disorders (16–20).…”

Section: Introductionmentioning

confidence: 99%

Association Between Interleukin-6 and Striatal Prediction-Error Signals Following Acute Stress in Healthy Female Participants

Treadway

Admon

Arulpragasam

et al. 2017

Biological Psychiatry

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Background Stress is widely known to alter behavioral responses to rewards and punishments. It is believed that stress may precipitate these changes through modulation of corticostriatal circuitry involved in reinforcement learning and motivation, although the intervening mechanisms remain unclear. One candidate is inflammation, which can rapidly increase following stress, and can disrupt dopamine-dependent reward pathways. Methods Here, in a sample of 88 healthy female participants, we first assessed the effect of an acute laboratory stress paradigm on levels of plasma interleukin-6 (IL-6), a cytokine known to be both responsive to stress and elevated in depression. In a second laboratory session, we examined the effects of a second laboratory stress paradigm on reward prediction error (RPE) signaling in the ventral striatum. Results We show that individual differences in stress-induced increases in IL-6 (session 1) were associated with decreased ventral striatal RPE signaling during reinforcement learning (session 2), though there was no main effect of stress on RPE. Further, changes in IL-6 following stress predicted intra-individual variability in perceived stress during a 4-month follow-up period. Conclusions Taken together, these data identify a novel link between IL-6 and striatal reward prediction errors during reinforcement learning in the context of acute psychological stress, as well as future appraisal of stressful life events.

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Section: Introductionmentioning

confidence: 99%

Association Between Interleukin-6 and Striatal Prediction-Error Signals Following Acute Stress in Healthy Female Participants

Treadway

Admon

Arulpragasam

et al. 2017

Biological Psychiatry

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“…Acute stress-related increases in glucocorticoids are critical both for the alarm signal as well as in regaining control over the stress signal resulting in healthy stress coping. Recent animal data show a glucocorticoid role in modulation of the medial PFC involved in goal-directed behaviors (54). Interestingly, the highly significant negative association between stress-related cortisol increases and reduced rACC/VmPFC was for the S-N average rACC/VmPFC response and not for the dynamic changes that were found to be correlated with active coping.…”

Section: Discussionmentioning

confidence: 92%

Dynamic neural activity during stress signals resilient coping

Sinha

Lacadie

Constable

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

195

164

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Active coping underlies a healthy stress response, but neural processes supporting such resilient coping are not well-known. Using a brief, sustained exposure paradigm contrasting highly stressful, threatening, and violent stimuli versus nonaversive neutral visual stimuli in a functional magnetic resonance imaging (fMRI) study, we show significant subjective, physiologic, and endocrine increases and temporally related dynamically distinct patterns of neural activation in brain circuits underlying the stress response. First, stressspecific sustained increases in the amygdala, striatum, hypothalamus, midbrain, right insula, and right dorsolateral prefrontal cortex (DLPFC) regions supported the stress processing and reactivity circuit. Second, dynamic neural activation during stress versus neutral runs, showing early increases followed by later reduced activation in the ventrolateral prefrontal cortex (VLPFC), dorsal anterior cingulate cortex (dACC), left DLPFC, hippocampus, and left insula, suggested a stress adaptation response network. Finally, dynamic stress-specific mobilization of the ventromedial prefrontal cortex (VmPFC), marked by initial hypoactivity followed by increased VmPFC activation, pointed to the VmPFC as a key locus of the emotional and behavioral control network. Consistent with this finding, greater neural flexibility signals in the VmPFC during stress correlated with active coping ratings whereas lower dynamic activity in the VmPFC also predicted a higher level of maladaptive coping behaviors in real life, including binge alcohol intake, emotional eating, and frequency of arguments and fights. These findings demonstrate acute functional neuroplasticity during stress, with distinct and separable brain networks that underlie critical components of the stress response, and a specific role for VmPFC neuroflexibility in stress-resilient coping.functional neuroimaging | stress | resilience coping | binge alcohol intake | emotional eating

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“…inhibition in AN-BP could reflect the consequences of prolonged, extreme stress, namely significantly low weight, which engenders various cognitive and neuroendocrine perturbations (57,58). Interestingly, preclinical research has identified disrupted dopaminergic signaling following severe stress (59,60); however, the effect of stress on dopaminergic projections to prefrontal cortex remains understudied. The dearth of research in this area discourages a premature interpretation of our stress induction effects in AN-BP.…”

Section: Stress-induced Reductions In Prefrontal Responses During Botmentioning

confidence: 99%

Prefrontal responses during proactive and reactive inhibition are differentially impacted by stress in anorexia and bulimia nervosa

Westwater

Mancini

Gorka

et al. 2020

Preprint

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Background: Binge-eating is a distressing, transdiagnostic eating disorder symptom associated with impulsivity, particularly in negative mood states. Neuroimaging studies of bulimia nervosa (BN) report reduced activity in fronto-striatal regions implicated in self-regulatory control. However, it remains unknown if negative affective states, including stress, impair self-regulation, and, if so, whether such self-regulatory deficits generalize to binge-eating in underweight individuals (i.e., the bingeing/purging subtype of anorexia nervosa; AN-BP). Methods:We determined the effect of acute stress on inhibitory control in 85 women (33 BN, 22 AN-BP, 30 matched controls). Participants underwent repeated functional MRI scanning, during performance of the stop-signal anticipation task, a validated measure of proactive (i.e., anticipation of stopping) and reactive (outright stopping) inhibition. Neural and behavioral responses to induced, psychological stress and a control task were evaluated on two separate days.Results: Women with BN had reduced proactive inhibition while prefrontal responses were increased in both AN-BP and BN. Reactive inhibition was neurally and behaviorally intact in both diagnostic groups. Both AN-BP and BN groups showed distinct, stress-induced changes in prefrontal activity during both proactive and reactive inhibition. However, task performance was not significantly affected by stress. Conclusions:These findings offer novel evidence of reduced proactive inhibition in BN, yet inhibitory control deficits did not generalize to AN-BP. While both groups showed altered neural responses during inhibition following stress, neither group demonstrated stress-induced performance deficits. As such, our findings counsel against a simplistic, stress-induced failure of regulation as a holistic explanation for binge-eating in these conditions.

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Stress effects on the neural substrates of motivated behavior

Cited by 106 publications

References 99 publications

Association Between Interleukin-6 and Striatal Prediction-Error Signals Following Acute Stress in Healthy Female Participants

Association Between Interleukin-6 and Striatal Prediction-Error Signals Following Acute Stress in Healthy Female Participants

Dynamic neural activity during stress signals resilient coping

Prefrontal responses during proactive and reactive inhibition are differentially impacted by stress in anorexia and bulimia nervosa

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