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A neural mechanism for affective well-being: Subgenual cingulate cortex mediates real-life effects of nonexercise activity on energy.

ABSTRACT: Physical activity substantially improves well-being and mental health, but the underlying brain processes remain unclear. Most research concerns exercise, although the majority of everyday human behaviors, such as walking or stair climbing, are nonexercise activities. Combining neuroimaging with ecological assessment of activity and GPS-triggered smartphone diaries, we show a specific association of nonexercise activity with energy in two independent samples mediated by the subgenual part of the anterior cingulate cortex (sgACC), a key emotion regulatory site. Furthermore, energy predicted a range of mental health metrics. sgACC volume moderated humans' emotional gain from nonexercise activity in real life: Individuals with low sgACC volume, a risk factor for depression, felt less energized when inactive but benefited more from periods of high nonexercise activity. This suggests an everyday life mechanism affecting affective well-being in the general population and, if substantiated in patient samples, a risk and resilience process for mood disorders.

SUBMITTER: Reichert M

PROVIDER: S-EPMC7673710 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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A neural mechanism for affective well-being: Subgenual cingulate cortex mediates real-life effects of nonexercise activity on energy.

Reichert Markus M Braun Urs U Gan Gabriela G Reinhard Iris I Giurgiu Marco M Ma Ren R Zang Zhenxiang Z Hennig Oliver O Koch Elena D ED Wieland Lena L Schweiger Janina J Inta Dragos D Hoell Andreas A Akdeniz Ceren C Zipf Alexander A Ebner-Priemer Ulrich W UW Tost Heike H Meyer-Lindenberg Andreas A

Science advances 20201106 45

Physical activity substantially improves well-being and mental health, but the underlying brain processes remain unclear. Most research concerns exercise, although the majority of everyday human behaviors, such as walking or stair climbing, are nonexercise activities. Combining neuroimaging with ecological assessment of activity and GPS-triggered smartphone diaries, we show a specific association of nonexercise activity with energy in two independent samples mediated by the subgenual part of the ...[more]

PMID: 33158875

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Project description:The subgenual anterior cingulate cortex is implicated in the pathology and treatment response of major depressive disorder. Low levels of brain-derived neurotrophic factor (BDNF) and reduced markers for GABA function, including in the amygdala, are reported in major depression, but their contribution to subgenual anterior cingulate cortex dysfunction is not known.Using polymerase chain reaction, we first assessed the degree to which BDNF controls mRNA expression (defined as BDNF dependency) of 15 genes relating to GABA and neuropeptide functions in the cingulate cortex of mice with reduced BDNF function (BDNF-heterozygous [Bdnf(+/-)] mice and BDNF exon-IV knockout [Bdnf(KIV)] mice). Gene expression was then quantified in the subgenual anterior cingulate cortex of 51 postmortem subjects with major depressive disorder and comparison subjects (total subjects, N=102; 49% were women) and compared with previous amygdala results.Based on the results in Bdnf(+/-) and Bdnf(KIV) mice, genes were sorted into high, intermediate, and no BDNF dependency sets. In postmortem human subjects with major depression, BDNF receptor (TRKB) expression, but not BDNF, was reduced. Postmortem depressed subjects exhibited down-regulation in genes with high and intermediate BDNF dependency, including markers of dendritic targeting interneurons (SST, NPY, and CORT) and a GABA synthesizing enzyme (GAD2). Changes extended to BDNF-independent genes (PVALB and GAD1). Changes were greater in men (potentially because of low baseline expression in women), displayed notable differences from prior amygdala results, and were not explained by demographic or clinical factors other than sex.These parallel human/mouse analyses provide direct (low TRKB) and indirect (low expression of BDNF-dependent genes) evidence in support of decreased BDNF signaling in the subgenual anterior cingulate cortex in individuals with major depressive disorder, implicate dendritic targeting GABA neurons and GABA synthesis, and, together, suggest a common BDNF-/GABA-related pathology in major depression with sex- and brain region-specific features.

Dataset Information

A neural mechanism for affective well-being: Subgenual cingulate cortex mediates real-life effects of nonexercise activity on energy.

Publications

A neural mechanism for affective well-being: Subgenual cingulate cortex mediates real-life effects of nonexercise activity on energy.

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