HCN2 Channels in Cholinergic Interneurons of Nucleus Accumbens Shell Regulate Depressive Behaviors

Neuron. 2019 Feb 20;101(4):662-672.e5. doi: 10.1016/j.neuron.2018.12.018. Epub 2019 Jan 10.

Abstract

Cholinergic interneurons (ChIs) in the nucleus accumbens (NAc) have been implicated in drug addiction, reward, and mood disorders. However, the physiological role of ChIs in depression has not been characterized. Here, we show that the tonic firing rate of ChIs in NAc shell is reduced in chronic stress mouse models and in a genetic mouse model of depression. Chemogenetic inhibition of NAc ChIs renders naive mice susceptible to stress, whereas enhancement of ChI activity reverses depressive phenotypes. As a component of the molecular mechanism, we found that the expression and function of the hyperpolarization-activated cyclic nucleotide-gated channel 2 (HCN2) are decreased in ChIs of NAc shell in depressed mice. Overexpression of HCN2 channels in ChIs enhances cell activity and is sufficient to rescue depressive phenotypes. These data suggest that enhancement of HCN2 channel activity in NAc ChIs is a feasible approach for the development of a new class of antidepressants.

Keywords: BacTRAP; DREADD; HCN2; MDD; cholinergic interneurons; mouse model of depression; nucleus accumbens; p11; shell and core; tonically active neurons.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials
  • Animals
  • Cholinergic Neurons / metabolism*
  • Cholinergic Neurons / physiology
  • Depressive Disorder / metabolism*
  • Depressive Disorder / physiopathology
  • Female
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / genetics
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / metabolism*
  • Interneurons / metabolism*
  • Interneurons / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Nucleus Accumbens / cytology
  • Nucleus Accumbens / metabolism*
  • Nucleus Accumbens / physiopathology

Substances

  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels