Monoaminergic orchestration of motor programs in a complex C. elegans behavior.

Monoaminergic orchestration of motor programs in a complex C. elegans behavior.
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DOI:
10.1371/journal.pbio.1001529
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发表时间:
2013
期刊:
影响因子:
9.8
通讯作者:
Alkema MJ
Alkema MJ
中科院分区:
生物学1区
文献类型:
--
作者:
Donnelly JL;Clark CM;Leifer AM;Pirri JK;Haburcak M;Francis MM;Samuel AD;Alkema MJ

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A single monoamine can orchestrate different phases of a compound motor sequence in C. elegans through the synaptic and extra-synaptic activation of distinct classes of receptors. 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. How the nervous system controls complex behaviors has intrigued neurobiologists for decades. There are many examples where sequential motor patterns of specific behaviors have been described in great detail. However, the neural mechanisms that orchestrate a full behavioral sequence are poorly understood. Gentle touch to the head of the roundworm C. elegans elicits an escape response in which the animal quickly moves backward. The reversal is followed by a deep turn that allows the animal to change its direction of locomotion and move away from the threatening stimulus. We found that the neurotransmitter tyramine controls the initial reversal phase of the escape response through the activation of a fast-acting ion channel and the later turning phase through the activation of a slow-acting G-protein coupled receptor (GPCR). We show that this tyramine GPCR is expressed in neurons that make contacts with the ventral muscles of the animal. Activation of this receptor facilitates the contraction of ventral muscles and thus allows the animal to turn and resume locomotion in the opposite direction during its escape. Our studies show how a single neurotransmitter coordinates sequential phases of a complex behavior through the activation of distinct classes of receptors.
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