Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior

Navonil Banerjee, Raja Bhattacharya, Michael Gorczyca, Kevin Collins, Michael M. Francis

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Animal behaviors are often composed of distinct alternating behavioral states. Neuromodulatory signals are thought to be critical for establishing stable behavioral states and for orchestrating transitions between them. However, we have only a limited understanding of how neuromodulatory systems act in vivo to alter circuit performance and shape behavior. To address these questions, we have investigated neuromodulatory signaling in the context of Caenorhabditis elegans egg-laying. Egg-laying activity cycles between discrete states–short bursts of egg deposition (active phases) that alternate with prolonged quiescent periods (inactive phases). Here using genetic, pharmacological and optogenetic approaches for cell-specific activation and inhibition, we show that a group of neurosecretory cells (uv1) located in close spatial proximity to the egg-laying neuromusculature direct the temporal organization of egg-laying by prolonging the duration of inactive phases. We demonstrate that the modulatory effects of the uv1 cells are mediated by peptides encoded by the nlp-7 and flp-11 genes that act locally to inhibit circuit activity, primarily by inhibiting vesicular release of serotonin from HSN motor neurons. This peptidergic inhibition is achieved, at least in part, by reducing synaptic vesicle abundance in the HSN motor neurons. By linking the in vivo actions of specific neuropeptide signaling systems with the generation of stable behavioral outcomes, our study reveals how cycles of neuromodulation emanating from non-neuronal cells can fundamentally shape the organization of a behavioral program.

Original languageEnglish (US)
Article numbere1006697
JournalPLoS Genetics
Volume13
Issue number4
DOIs
StatePublished - Apr 1 2017

Fingerprint

neuropeptides
Neuropeptides
Ovum
oviposition
egg
motor neurons
Motor Neurons
neurosecretory cells
Optogenetics
Activity Cycles
cells
Caenorhabditis elegans
Animal Behavior
serotonin
animal behavior
Synaptic Vesicles
vesicle
peptide
peptides
Serotonin

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior. / Banerjee, Navonil; Bhattacharya, Raja; Gorczyca, Michael; Collins, Kevin; Francis, Michael M.

In: PLoS Genetics, Vol. 13, No. 4, e1006697, 01.04.2017.

Research output: Contribution to journalArticle

Banerjee, Navonil ; Bhattacharya, Raja ; Gorczyca, Michael ; Collins, Kevin ; Francis, Michael M. / Local neuropeptide signaling modulates serotonergic transmission to shape the temporal organization of C. elegans egg-laying behavior. In: PLoS Genetics. 2017 ; Vol. 13, No. 4.
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