Excitation of medium spiny neurons by 'inhibitory' ultrapotent chemogenetics via shifts in chloride reversal potential.

Gantz, Stephanie C; Ortiz, Maria M; Belilos, Andrew J; Moussawi, Khaled · Elife · 2021

basic_science · Level V

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Abstract

Ultrapotent chemogenetics, including the chloride-permeable inhibitory PSAM<sup>4</sup>-GlyR receptor, were recently proposed as a powerful strategy to selectively control neuronal activity in awake, behaving animals. We aimed to validate the inhibitory function of PSAM<sup>4</sup>-GlyR in dopamine D1 receptor-expressing medium spiny neurons (D1-MSNs) in the ventral striatum. Activation of PSAM<sup>4</sup>-GlyR with the uPSEM<sup>792</sup> ligand enhanced rather than suppressed the activity of D1-MSNs in vivo as indicated by increased c-fos expression in D1-MSNs and in vitro as indicated by cell-attached recordings from D1-MSNs in mouse brain slices. Whole-cell recordings showed that activation of PSAM<sup>4</sup>-GlyR depolarized D1-MSNs, attenuated GABAergic inhibition, and shifted the reversal potential of PSAM<sup>4</sup>-GlyR current to more depolarized potentials, perpetuating the depolarizing effect of receptor activation. These data show that 'inhibitory' PSAM<sup>4</sup>-GlyR chemogenetics may activate certain cell types and highlight the pitfalls of utilizing chloride conductances to inhibit neurons.

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