Amygdala-Midbrain Connections Modulate Appetitive and Aversive Learning

Elizabeth E. Steinberg, Felicity Gore, Boris D. Heifets, Madison D. Taylor, Zane C. Norville, Kevin T. Beier, Csaba Földy, Talia N. Lerner, Liqun Luo, Karl Deisseroth, Robert C. Malenka*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

8 Scopus citations

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. Steinberg et al. investigate how connections between the central amygdala and the lateral substantia nigra contribute to emotional behaviors. They find that amygdalonigral neurons are activated by salient stimuli and participate in appetitive and aversive learning via connections with nigral GABA and dopamine neurons.

Original languageEnglish (US)
Pages (from-to)1026-1043.e9
JournalNeuron
Volume106
Issue number6
DOIs
StatePublished - Jun 17 2020
Externally publishedYes

Keywords

  • Pavlovian
  • aversion
  • central amygdala
  • dopamine
  • instrumental
  • reinforcement learning
  • reward
  • salience
  • substantia nigra

ASJC Scopus subject areas

  • Neuroscience(all)

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