Stress gates an astrocytic energy reservoir to impair synaptic plasticity

Ciaran Murphy-Royal, April D. Johnston, Andrew K. J. Boyce, Blanca Diaz-Castro, Adam Institoris, Govind Peringod, Oliver Zhang, Randy F. Stout, David C. Spray, Roger J. Thompson, Baljit S. Khakh, Jaideep S. Bains and Grant R. Gordon ()
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Ciaran Murphy-Royal: University of Calgary
April D. Johnston: University of California Los Angeles, UCLA
Andrew K. J. Boyce: University of Calgary
Blanca Diaz-Castro: University of California Los Angeles, UCLA
Adam Institoris: University of Calgary
Govind Peringod: University of Calgary
Oliver Zhang: University of Calgary
Randy F. Stout: New York Institute of Technology College of Osteopathic Medicine
David C. Spray: Albert Einstein College of Medicine
Roger J. Thompson: University of Calgary
Baljit S. Khakh: University of California Los Angeles, UCLA
Jaideep S. Bains: University of Calgary
Grant R. Gordon: University of Calgary

Nature Communications, 2020, vol. 11, issue 1, 1-18

Abstract: Abstract Astrocytes support the energy demands of synaptic transmission and plasticity. Enduring changes in synaptic efficacy are highly sensitive to stress, yet whether changes to astrocyte bioenergetic control of synapses contributes to stress-impaired plasticity is unclear. Here we show in mice that stress constrains the shuttling of glucose and lactate through astrocyte networks, creating a barrier for neuronal access to an astrocytic energy reservoir in the hippocampus and neocortex, compromising long-term potentiation. Impairing astrocytic delivery of energy substrates by reducing astrocyte gap junction coupling with dominant negative connexin 43 or by disrupting lactate efflux was sufficient to mimic the effects of stress on long-term potentiation. Furthermore, direct restoration of the astrocyte lactate supply alone rescued stress-impaired synaptic plasticity, which was blocked by inhibiting neural lactate uptake. This gating of synaptic plasticity in stress by astrocytic metabolic networks indicates a broader role of astrocyte bioenergetics in determining how experience-dependent information is controlled.

Date: 2020
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DOI: 10.1038/s41467-020-15778-9

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