Glutamatergic and GABAergic neurons in pontine central gray mediate opposing valence-specific behaviors through a global network

Neuron. 2023 May 3;111(9):1486-1503.e7. doi: 10.1016/j.neuron.2023.02.012. Epub 2023 Mar 8.

Abstract

Extracting the valence of environmental cues is critical for animals' survival. How valence in sensory signals is encoded and transformed to produce distinct behavioral responses remains not well understood. Here, we report that the mouse pontine central gray (PCG) contributes to encoding both negative and positive valences. PCG glutamatergic neurons were activated selectively by aversive, but not reward, stimuli, whereas its GABAergic neurons were preferentially activated by reward signals. The optogenetic activation of these two populations resulted in avoidance and preference behavior, respectively, and was sufficient to induce conditioned place aversion/preference. Suppression of them reduced sensory-induced aversive and appetitive behaviors, respectively. These two functionally opponent populations, receiving a broad range of inputs from overlapping yet distinct sources, broadcast valence-specific information to a distributed brain network with distinguishable downstream effectors. Thus, PCG serves as a critical hub to process positive and negative valences of incoming sensory signals and drive valence-specific behaviors with distinct circuits.

Keywords: aversion and reward; dorsal pons; emotional processing; glutamatergic and GABAergic neurons; motivated behavior; neural circuits for behaviors; sensory responses; valence coding; valence processing.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Affect
  • Animals
  • Brain*
  • Cues
  • GABAergic Neurons*
  • Mice
  • Periaqueductal Gray