Voluntary Wheel Running Exercise Evoked by Food-Restriction Stress Exacerbates Weight Loss of Adolescent Female Rats But Also Promotes Resilience by Enhancing GABAergic Inhibition of Pyramidal Neurons in the Dorsal Hippocampus

Overview

Journal Cereb Cortex

Publisher Oxford University Press

Specialty Neurology

Date 2018 Nov 22

PMID 30462186

Citations 5

Authors

Tara G Chowdhury

Gauri S Wable

Yi-Wen Chen

Kei Tateyama

Irene Yu

Jia-Yi Wang

Alex D Reyes

Chiye Aoki

Affiliations

Soon will be listed here.

Abstract

Adolescence is marked by increased vulnerability to mental disorders and maladaptive behaviors, including anorexia nervosa. Food-restriction (FR) stress evokes foraging, which translates to increased wheel running exercise (EX) for caged rodents, a maladaptive behavior, since it does not improve food access and exacerbates weight loss. While almost all adolescent rodents increase EX following FR, some then become resilient by suppressing EX by the second-fourth FR day, which minimizes weight loss. We asked whether GABAergic plasticity in the hippocampus may underlie this gain in resilience. In vitro slice physiology revealed doubling of pyramidal neurons' GABA response in the dorsal hippocampus of food-restricted animals with wheel access (FR + EX for 4 days), but without increase of mIPSC amplitudes. mIPSC frequency increased by 46%, but electron microscopy revealed no increase in axosomatic GABAergic synapse number onto pyramidal cells and only a modest increase (26%) of GABAergic synapse lengths. These changes suggest increase of vesicular release probability and extrasynaptic GABAA receptors and unsilencing of GABAergic synapses. GABAergic synapse lengths correlated with individual's suppression of wheel running and weight loss. These analyses indicate that EX can have dual roles-exacerbate weight loss but also promote resilience to some by dampening hippocampal excitability.

Citing Articles

Running from Stress: Neurobiological Mechanisms of Exercise-Induced Stress Resilience.

Nowacka-Chmielewska M, Grabowska K, Grabowski M, Meybohm P, Burek M, Malecki A Int J Mol Sci. 2022; 23(21).

PMID: 36362131 PMC: 9654650. DOI: 10.3390/ijms232113348.

Pathway-specific GABAergic inhibition contributes to the gain of resilience against anorexia-like behavior of adolescent female mice.

Aoki C, Santiago A Front Behav Neurosci. 2022; 16:990354.

PMID: 36311865 PMC: 9606475. DOI: 10.3389/fnbeh.2022.990354.

GABAergic interneurons' feedback inhibition of dorsal raphe-projecting pyramidal neurons of the medial prefrontal cortex suppresses feeding of adolescent female mice undergoing activity-based anorexia.

Du M, Santiago A, Akiz C, Aoki C Brain Struct Funct. 2022; 227(6):2127-2151.

PMID: 35635653 PMC: 9277364. DOI: 10.1007/s00429-022-02507-9.

Genetics and neurobiology of eating disorders.

Bulik C, Coleman J, Hardaway J, Breithaupt L, Watson H, Bryant C Nat Neurosci. 2022; 25(5):543-554.

PMID: 35524137 PMC: 9744360. DOI: 10.1038/s41593-022-01071-z.

Voluntary wheel running promotes myelination in the motor cortex through Wnt signaling in mice.

Zheng J, Sun X, Ma C, Li B, Luo F Mol Brain. 2019; 12(1):85.

PMID: 31651333 PMC: 6814131. DOI: 10.1186/s13041-019-0506-8.

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