Monoaminergic Orchestration of Motor Programs in a Complex C. elegans Behavior

Jamie L. Donnelly, Christopher M. Clark, Andrew Michael Leifer, Jennifer K. Pirri, Marian Haburcak, Michael M. Francis, Aravinthan D.T. Samuel, Mark J. Alkema

Research output: Contribution to journalArticle

50 Citations (Scopus)

Abstract

Monoamines provide chemical codes of behavioral states. However, the neural mechanisms of monoaminergic orchestration of behavior are poorly understood. Touch elicits an escape response in Caenorhabditis elegans where the animal moves backward and turns to change its direction of locomotion. We show that the tyramine receptor SER-2 acts through a Gαo pathway to inhibit neurotransmitter release from GABAergic motor neurons that synapse onto ventral body wall muscles. Extrasynaptic activation of SER-2 facilitates ventral body wall muscle contraction, contributing to the tight ventral turn that allows the animal to navigate away from a threatening stimulus. Tyramine temporally coordinates the different phases of the escape response through the synaptic activation of the fast-acting ionotropic receptor, LGC-55, and extrasynaptic activation of the slow-acting metabotropic receptor, SER-2. Our studies show, at the level of single cells, how a sensory input recruits the action of a monoamine to change neural circuit properties and orchestrate a compound motor sequence.

Original languageEnglish (US)
Article numbere1001529
JournalPLoS biology
Volume11
Issue number4
DOIs
StatePublished - Apr 1 2013

Fingerprint

monoamines
tyramine
Chemical activation
integument
GABAergic Neurons
Tyramine
receptors
Muscle
Caenorhabditis elegans
Touch
Animals
Motor Neurons
Locomotion
Muscle Contraction
Synapses
Neurotransmitter Agents
muscle contraction
touch (sensation)
synapse
motor neurons

All Science Journal Classification (ASJC) codes

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Neuroscience(all)

Cite this

Donnelly, J. L., Clark, C. M., Leifer, A. M., Pirri, J. K., Haburcak, M., Francis, M. M., ... Alkema, M. J. (2013). Monoaminergic Orchestration of Motor Programs in a Complex C. elegans Behavior. PLoS biology, 11(4), [e1001529]. https://doi.org/10.1371/journal.pbio.1001529
Donnelly, Jamie L. ; Clark, Christopher M. ; Leifer, Andrew Michael ; Pirri, Jennifer K. ; Haburcak, Marian ; Francis, Michael M. ; Samuel, Aravinthan D.T. ; Alkema, Mark J. / Monoaminergic Orchestration of Motor Programs in a Complex C. elegans Behavior. In: PLoS biology. 2013 ; Vol. 11, No. 4.
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Donnelly, JL, Clark, CM, Leifer, AM, Pirri, JK, Haburcak, M, Francis, MM, Samuel, ADT & Alkema, MJ 2013, 'Monoaminergic Orchestration of Motor Programs in a Complex C. elegans Behavior' PLoS biology, vol. 11, no. 4, e1001529. https://doi.org/10.1371/journal.pbio.1001529

Monoaminergic Orchestration of Motor Programs in a Complex C. elegans Behavior. / Donnelly, Jamie L.; Clark, Christopher M.; Leifer, Andrew Michael; Pirri, Jennifer K.; Haburcak, Marian; Francis, Michael M.; Samuel, Aravinthan D.T.; Alkema, Mark J.

In: PLoS biology, Vol. 11, No. 4, e1001529, 01.04.2013.

Research output: Contribution to journalArticle

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