Transient cAMP production drives rapid and sustained spiking in brainstem parabrachial neurons to suppress feeding

Neuron. 2024 May 1;112(9):1416-1425.e5. doi: 10.1016/j.neuron.2024.02.002. Epub 2024 Feb 27.

Abstract

Brief stimuli can trigger longer-lasting brain states. G-protein-coupled receptors (GPCRs) could help sustain such states by coupling slow-timescale molecular signals to neuronal excitability. Brainstem parabrachial nucleus glutamatergic (PBNGlut) neurons regulate sustained brain states such as pain and express Gs-coupled GPCRs that increase cAMP signaling. We asked whether cAMP in PBNGlut neurons directly influences their excitability and effects on behavior. Both brief tail shocks and brief optogenetic stimulation of cAMP production in PBNGlut neurons drove minutes-long suppression of feeding. This suppression matched the duration of prolonged elevations in cAMP, protein kinase A (PKA) activity, and calcium activity in vivo and ex vivo, as well as sustained, PKA-dependent increases in action potential firing ex vivo. Shortening this elevation in cAMP reduced the duration of feeding suppression following tail shocks. Thus, molecular signaling in PBNGlut neurons helps prolong neural activity and behavioral states evoked by brief, salient bodily stimuli.

Keywords: GPCR; brain slice imaging; cAMP; calcium imaging; electrophysiology; feeding; fluorescent biosensor imaging; in vivo; licking; neuronal activity; parabrachial nucleus; protein kinase A; two-photon microscopy.

Publication types

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

MeSH terms

  • Action Potentials* / physiology
  • Animals
  • Brain Stem / metabolism
  • Brain Stem / physiology
  • Cyclic AMP* / metabolism
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Feeding Behavior* / physiology
  • Female
  • Glutamic Acid / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons* / metabolism
  • Neurons* / physiology
  • Optogenetics
  • Parabrachial Nucleus* / metabolism
  • Parabrachial Nucleus* / physiology

Substances

  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Glutamic Acid