Amygdala-Midbrain Connections Modulate Appetitive and Aversive Learning

Neuron. 2020 Jun 17;106(6):1026-1043.e9. doi: 10.1016/j.neuron.2020.03.016. Epub 2020 Apr 14.

Abstract

The central amygdala (CeA) orchestrates adaptive responses to emotional events. While CeA substrates for defensive behaviors have been studied extensively, CeA circuits for appetitive behaviors and their relationship to threat-responsive circuits remain poorly defined. Here, we demonstrate that the CeA sends robust inhibitory projections to the lateral substantia nigra (SNL) that contribute to appetitive and aversive learning in mice. CeA→SNL neural responses to appetitive and aversive stimuli were modulated by expectation and magnitude consistent with a population-level salience signal, which was required for Pavlovian conditioned reward-seeking and defensive behaviors. CeA→SNL terminal activation elicited reinforcement when linked to voluntary actions but failed to support Pavlovian associations that rely on incentive value signals. Consistent with a disinhibitory mechanism, CeA inputs preferentially target SNL GABA neurons, and CeA→SNL and SNL dopamine neurons respond similarly to salient stimuli. Collectively, our results suggest that amygdala-nigra interactions represent a previously unappreciated mechanism for influencing emotional behaviors.

Keywords: Pavlovian; aversion; central amygdala; dopamine; instrumental; reinforcement learning; reward; salience; substantia nigra.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Appetitive Behavior / physiology*
  • Avoidance Learning / physiology*
  • Central Amygdaloid Nucleus / physiology*
  • Conditioning, Classical / physiology
  • Dopaminergic Neurons / physiology*
  • Emotions
  • GABAergic Neurons / physiology*
  • Mice
  • Neural Pathways
  • Reinforcement, Psychology
  • Reward
  • Substantia Nigra / cytology
  • Substantia Nigra / physiology*