State-specific gating of salient cues by midbrain dopaminergic input to basal amygdala

Nat Neurosci. 2019 Nov;22(11):1820-1833. doi: 10.1038/s41593-019-0506-0. Epub 2019 Oct 14.

Abstract

Basal amygdala (BA) neurons guide associative learning via acquisition of responses to stimuli that predict salient appetitive or aversive outcomes. We examined the learning- and state-dependent dynamics of BA neurons and ventral tegmental area (VTA) dopamine (DA) axons that innervate BA (VTADA→BA) using two-photon imaging and photometry in behaving mice. BA neurons did not respond to arbitrary visual stimuli, but acquired responses to stimuli that predicted either rewards or punishments. Most VTADA→BA axons were activated by both rewards and punishments, and they acquired responses to cues predicting these outcomes during learning. Responses to cues predicting food rewards in VTADA→BA axons and BA neurons in hungry mice were strongly attenuated following satiation, while responses to cues predicting unavoidable punishments persisted or increased. Therefore, VTADA→BA axons may provide a reinforcement signal of motivational salience that invigorates adaptive behaviors by promoting learned responses to appetitive or aversive cues in distinct, intermingled sets of BA excitatory neurons.

Publication types

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

MeSH terms

  • Amygdala / physiology*
  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Cues
  • Dopamine Plasma Membrane Transport Proteins / genetics
  • Dopaminergic Neurons / physiology*
  • Female
  • Male
  • Mice
  • Mice, Transgenic
  • Neural Pathways / physiology
  • Photic Stimulation
  • Punishment
  • Reward
  • Sensory Gating / physiology*
  • Ventral Tegmental Area / physiology*
  • Visual Perception / physiology

Substances

  • Dopamine Plasma Membrane Transport Proteins
  • Slc6a3 protein, mouse
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2