Reward signaling in a recurrent circuit of dopaminergic neurons and peptidergic Kenyon cells

Nat Commun. 2019 Jul 15;10(1):3097. doi: 10.1038/s41467-019-11092-1.

Abstract

Dopaminergic neurons in the brain of the Drosophila larva play a key role in mediating reward information to the mushroom bodies during appetitive olfactory learning and memory. Using optogenetic activation of Kenyon cells we provide evidence that recurrent signaling exists between Kenyon cells and dopaminergic neurons of the primary protocerebral anterior (pPAM) cluster. Optogenetic activation of Kenyon cells paired with odor stimulation is sufficient to induce appetitive memory. Simultaneous impairment of the dopaminergic pPAM neurons abolishes appetitive memory expression. Thus, we argue that dopaminergic pPAM neurons mediate reward information to the Kenyon cells, and in turn receive feedback from Kenyon cells. We further show that this feedback signaling is dependent on short neuropeptide F, but not on acetylcholine known to be important for odor-shock memories in adult flies. Our data suggest that recurrent signaling routes within the larval mushroom body circuitry may represent a mechanism subserving memory stabilization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcholine / metabolism
  • Animals
  • Appetite / physiology
  • Brain / cytology
  • Brain / physiology*
  • Conditioning, Classical
  • Dopaminergic Neurons / physiology*
  • Drosophila melanogaster / physiology*
  • Feedback, Physiological
  • Larva
  • Memory / physiology*
  • Models, Psychological
  • Mushroom Bodies / cytology
  • Mushroom Bodies / physiology*
  • Neural Pathways / physiology
  • Neuropeptides / metabolism
  • Odorants
  • Olfactory Perception / physiology
  • Optogenetics
  • Reward*

Substances

  • Neuropeptides
  • neuropeptide F
  • Acetylcholine