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Controllability over stressor decreases responses in key threat-related brain areas.

ABSTRACT: Controllability over stressors has major impacts on brain and behavior. In humans, however, the effect of controllability on responses to stressors is poorly understood. Using functional magnetic resonance imaging (fMRI), we investigated how controllability altered responses to a shock-plus-sound stressor with a between-group yoked design, where participants in controllable and uncontrollable groups experienced matched stressor exposure. Employing Bayesian multilevel analysis at the level of regions of interest and voxels in the insula, and standard voxelwise analysis, we found that controllability decreased stressor-related responses across threat-related regions, notably in the bed nucleus of the stria terminalis and anterior insula. Posterior cingulate cortex, posterior insula, and possibly medial frontal gyrus showed increased responses during control over stressor. Our findings support the idea that the aversiveness of stressors is reduced when controllable, leading to decreased responses across key regions involved in anxiety-related processing, even at the level of the extended amygdala.

SUBMITTER: Limbachia C

PROVIDER: S-EPMC7785729 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Controllability over stressor decreases responses in key threat-related brain areas.

Limbachia Chirag C Morrow Kelly K Khibovska Anastasiia A Meyer Christian C Padmala Srikanth S Pessoa Luiz L

Communications biology 20210105 1

Controllability over stressors has major impacts on brain and behavior. In humans, however, the effect of controllability on responses to stressors is poorly understood. Using functional magnetic resonance imaging (fMRI), we investigated how controllability altered responses to a shock-plus-sound stressor with a between-group yoked design, where participants in controllable and uncontrollable groups experienced matched stressor exposure. Employing Bayesian multilevel analysis at the level of reg ...[more]

PMID: 33402686

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Project description:BackgroundIn humans the stress response is known to be modulated to a great extent by psychological factors, particularly by the predictability and the perceived control that the subject has of the stressor. This psychological dimension of the stress response has also been demonstrated in animals phylogenetically closer to humans (i.e. mammals). However, its occurrence in fish, which represent a divergent vertebrate evolutionary lineage from that of mammals, has not been established yet, and, if present, would indicate a deep evolutionary origin of these mechanisms across vertebrates. Moreover, the fact that psychological modulation of stress is implemented in mammals by a brain cortical top-down inhibitory control over subcortical stress-responsive structures, and the absence of a brain cortex in fish, has been used as an argument against the possibility of psychological stress in fish, with implications for the assessment of fish sentience and welfare. Here, we have investigated the occurrence of psychological stress in fish by assessing how stressor controllability modulates the stress response in European seabass (Dicentrarchus labrax).ResultsFish were exposed to either a controllable or an uncontrollable stressor (i.e. possibility or impossibility to escape a signaled stressor). The effect of loss of control (possibility to escape followed by impossibility to escape) was also assessed. Both behavioral and circulating cortisol data indicates that the perception of control reduces the response to the stressor, when compared to the uncontrollable situation. Losing control had the most detrimental effect. The brain activity of the teleost homologues to the sensory cortex (Dld) and hippocampus (Dlv) parallels the uncontrolled and loss of control stressors, respectively, whereas the activity of the lateral septum (Vv) homologue responds in different ways depending on the gene marker of brain activity used.ConclusionsThese results suggest the psychological modulation of the stress response to be evolutionary conserved across vertebrates, despite being implemented by different brain circuits in mammals (pre-frontal cortex) and fish (Dld-Dlv).

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Controllability over stressor decreases responses in key threat-related brain areas.

Publications

Controllability over stressor decreases responses in key threat-related brain areas.

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