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

Author:

Chowdhury Tara G1,Wable Gauri S1,Chen Yi-Wen1,Tateyama Kei1,Yu Irene1,Wang Jia-Yi1,Reyes Alex D1,Aoki Chiye12ORCID

Affiliation:

1. Center for Neural Science, NYU, New York, NY, USA

2. The Neuroscience Institute, NYU Langone Medical Center, New York, NY, USA

Abstract

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.

Funder

The Klarman Foundation Grant Program in Eating Disorders Research

National Institutes of Health

NYU’s Research Challenge Fund

Fulbright Graduate Study Grant

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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