Stress-induced plasticity of a CRH/GABA projection disrupts reward behaviors in mice

Matthew T. Birnie, Annabel K. Short, Gregory B. Carvalho, Lara Taniguchi, Benjamin G. Gunn, Aidan L. Pham, Christy A. Itoga, Xiangmin Xu, Lulu Y. Chen, Stephen V. Mahler, Yuncai Chen () and Tallie Z. Baram ()
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Matthew T. Birnie: University of California-Irvine
Annabel K. Short: University of California-Irvine
Gregory B. Carvalho: University of California-Irvine
Lara Taniguchi: University of California-Irvine
Benjamin G. Gunn: University of California-Irvine
Aidan L. Pham: University of California-Irvine
Christy A. Itoga: University of California-Irvine
Xiangmin Xu: University of California-Irvine
Lulu Y. Chen: University of California-Irvine
Stephen V. Mahler: University of California-Irvine
Yuncai Chen: University of California-Irvine
Tallie Z. Baram: University of California-Irvine

Nature Communications, 2023, vol. 14, issue 1, 1-10

Abstract: Abstract Disrupted operations of the reward circuit underlie major emotional disorders, including depression, which commonly arise following early life stress / adversity (ELA). However, how ELA enduringly impacts reward circuit functions remains unclear. We characterize a stress-sensitive projection connecting basolateral amygdala (BLA) and nucleus accumbens (NAc) that co-expresses GABA and the stress-reactive neuropeptide corticotropin-releasing hormone (CRH). We identify a crucial role for this projection in executing disrupted reward behaviors provoked by ELA: chemogenetic and optogenetic stimulation of the projection in control male mice suppresses several reward behaviors, recapitulating deficits resulting from ELA and demonstrating the pathway’s contributions to normal reward behaviors. In adult ELA mice, inhibiting–but not stimulating–the projection, restores typical reward behaviors yet has little effect in controls, indicating ELA-induced maladaptive plasticity of this reward-circuit component. Thus, we discover a stress-sensitive, reward inhibiting BLA → NAc projection with unique molecular features, which may provide intervention targets for disabling mental illnesses.

Date: 2023
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DOI: 10.1038/s41467-023-36780-x

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