Sex differences in the effect of acute fasting on excitatory and inhibitory synapses onto ventral tegmental area dopamine neurons.

dopamine endocannabinoid excitatory synaptic transmission fasting inhibitory synaptic transmission ventral tegmental area

Journal

The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262

Informations de publication

Date de publication:
12 2020
Historique:
received: 25 06 2020
accepted: 01 09 2020
pubmed: 5 9 2020
medline: 2 3 2021
entrez: 4 9 2020
Statut: ppublish

Résumé

Fasting can increase motivation for food and can energize reward-seeking. Ventral tegmental area (VTA) dopamine neurons respond to motivationally relevant information and fasting can influence mesolimbic dopamine concentration. An acute overnight fast differentially alters food approach behaviours and excitatory synaptic transmission onto VTA dopamine neurons of male or female mice. While inhibitory synapses onto VTA dopamine neurons are not altered by fasting in male or female mice, male mice had strengthened excitatory synapses whereas female mice had increased endocannabinoid-mediated short-term plasticity at excitatory synapses. These results help us understand how fasting differentially influences excitatory synaptic transmission onto dopamine neurons and may inform different strategies for fasting-induced food seeking by male and female mice. Dopamine neurons in the ventral tegmental area (VTA) are important for energizing goal-directed behaviour towards food and are sensitive to changes in metabolic states. Fasting increases the incentive motivation for food and the mobilization of energy stores and has sex-dependent effects. However, it is unknown how acute fasting alters excitatory or inhibitory synaptic transmission onto VTA dopamine neurons. An acute 16 h overnight fast induced increased food-seeking behaviour that was more predominant in male mice. Fasting increased miniature excitatory postsynaptic current frequency and amplitude in male, but not female, mice. This effect was not due to altered release probability as there was no change in the paired pulse ratio, nor was it due to an altered postsynaptic response as there was no change in the AMPA receptor/NMDA receptor ratio or response to glutamate uncaging. However, this effect was consistent with an increase in the number of release sites. In addition, depolarization-induced suppression of excitation, a measure of short-term endocannabinoid-mediated plasticity, was enhanced in female but not male fasted mice. There were no fasting-induced changes at inhibitory synapses onto dopamine neurons of male or female mice. Taken together, these results demonstrate that fasting influences excitatory synapses differentially in male and female mice, but preserves inhibitory synapses onto dopamine neurons, indicating that the mesolimbic circuits of male and female mice respond differently to acute energy deprivation.

Identifiants

pubmed: 32886798
doi: 10.1113/JP280412
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5523-5539

Subventions

Organisme : CIHR
ID : FDN148473
Pays : Canada

Informations de copyright

© 2020 The Authors. The Journal of Physiology © 2020 The Physiological Society.

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Auteurs

Nathan Godfrey (N)

Department of Physiology and Pharmacology, University of Calgary, Calgary, Alberta, Canada.

Stephanie L Borgland (SL)

Department of Physiology and Pharmacology, University of Calgary, Calgary, Alberta, Canada.

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