Natural and Drug Rewards Engage Distinct Pathways that Converge on Coordinated Hypothalamic and Reward Circuits

Neuron. 2019 Sep 4;103(5):891-908.e6. doi: 10.1016/j.neuron.2019.05.050. Epub 2019 Jul 2.

Abstract

Motivated behavior is influenced by neural networks that integrate physiological needs. Here, we describe coordinated regulation of hypothalamic feeding and midbrain reward circuits in awake behaving mice. We find that alcohol and other non-nutritive drugs inhibit activity in hypothalamic feeding neurons. Interestingly, nutrients and drugs utilize different pathways for the inhibition of hypothalamic neuron activity, as alcohol signals hypothalamic neurons in a vagal-independent manner, while fat and satiation signals require the vagus nerve. Concomitantly, nutrients, alcohol, and drugs also increase midbrain dopamine signaling. We provide evidence that these changes are interdependent, as modulation of either hypothalamic neurons or midbrain dopamine signaling influences reward-evoked activity changes in the other population. Taken together, our results demonstrate that (1) food and drugs can engage at least two peripheral→central pathways to influence hypothalamic neuron activity, and (2) hypothalamic and dopamine circuits interact in response to rewards.

Publication types

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

MeSH terms

  • Agouti-Related Protein / metabolism
  • Amphetamine / pharmacology
  • Animals
  • Central Nervous System Depressants / pharmacology*
  • Cocaine / pharmacology
  • Dopamine Antagonists / pharmacology
  • Dopamine Uptake Inhibitors / pharmacology*
  • Dopaminergic Neurons / drug effects*
  • Dopaminergic Neurons / metabolism
  • Ethanol / pharmacology*
  • Feeding Behavior / drug effects*
  • Hypothalamus / drug effects*
  • Hypothalamus / metabolism
  • Mice
  • Neural Pathways / drug effects
  • Neurons / drug effects
  • Neurons / metabolism
  • Nicotine / pharmacology
  • Nicotinic Agonists / pharmacology*
  • Pro-Opiomelanocortin / metabolism
  • Reward*
  • Vagotomy
  • Vagus Nerve / physiology

Substances

  • Agouti-Related Protein
  • Central Nervous System Depressants
  • Dopamine Antagonists
  • Dopamine Uptake Inhibitors
  • Nicotinic Agonists
  • Ethanol
  • Pro-Opiomelanocortin
  • Nicotine
  • Amphetamine
  • Cocaine