Abstract
Caenorhabditis elegans male copulation requires coordinated temporal-spatial execution of different motor outputs. During mating, a cloacal circuit consisting of cholinergic sensory-motor neurons and sex muscles maintains the male's position and executes copulatory spicule thrusts at his mate's vulva. However, distinct signaling mechanisms that delimit these behaviors to their proper context are unclear. We found that dopamine (DA) signaling directs copulatory spicule insertion attempts to the hermaphrodite vulva by dampening spurious stimulus-independent sex muscle contractions. From pharmacology and genetic analyses, DA antagonizes stimulatory ACh signaling via the D2-like receptors, DOP-2 and DOP-3, and Gαo/i proteins, GOA-1 and GPA-7. Calcium imaging and optogenetics suggest that heightened DA-expressing ray neuron activities coincide with the cholinergic cloacal ganglia function during spicule insertion attempts. D2-like receptor signaling also attenuates the excitability of additional mating circuits to reduce the duration of mating attempts with unproductive and/or inappropriate partners. This suggests that, during wild-type mating, simultaneous DA-ACh signaling modulates the activity threshold of repetitive motor programs, thus confining the behavior to the proper situational context.
Highlights
Context-dependent motor patterns are the outcome of unique interplay amongst neuromodulators in the central nervous system (CNS)
An animal’s behavior is a complex output displayed in response to diverse external cues, which are sensed and processed by the nervous system
The neurotransmitter dopamine (DA) is involved in adjusting animal movements, DA neurotransmission is a candidate for coupling behaviors to the proper situational context
Summary
Context-dependent motor patterns are the outcome of unique interplay amongst neuromodulators in the central nervous system (CNS). The neurotransmitter dopamine (DA) modulates gammaaminobutyric acid (GABA), glutamate and acetylcholine (ACh) activity in cognitive and motor behaviors [1,2,3,4,5,6]. DA adjusts motor outputs by selective synergy/antagonism of tiered neuronal population’s activities [2,7]. In the brain this regulation is initiated by DA secretion from the substantia nigra, which antagonizes post-synaptic cholinergic striatal interneurons [8]. Vertebrate and invertebrate models that fully encompass the in vivo cellular and molecular components of the DA-ACh interaction, which refine motor outputs, remain elusive
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