Abstract
BackgroundMost rhythmic motor behaviors in nature are episodic i.e. they alternate between different behavioral states, including quiescence. Electrophysiological studies in invertebrate behavioral switching, maintenance and quiescence have elucidated several neuronal mechanisms that generate a temporal pattern in behavior. However, the genetic bases of these processes are less well studied. We have previously uncovered a novel episodic behavior exhibited by C. elegans in liquid media where they alternate between distinct phases of rhythmic swimming and quiescence. Here, we have investigated the effect of several genes and their site of action on the behavioral quiescence exhibited in liquid by the nematode C. elegans.ResultsWe have previously reported that high cholinergic signaling promotes quiescence and command interneurons are critical for timing the quiescence bout durations. We have found that in addition to command interneurons, sensory neurons are also critical for quiescence. We show that the protein phosphatase calcineurin homolog tax-6 promotes swimming whereas the protein kinase G homolog egl-4 promotes quiescence. tax-6 expression in the sensory neurons is sufficient to account for its effect. egl-4 also acts in multiple sensory neurons to mediate its effect on quiescence. In addition our data is consistent with regulation of quiescence by egl-4 acting functionally downstream of release of acetylcholine (ACh) by motor neurons.ConclusionsOur study provides genetic evidence for mechanisms underlying the maintenance of a behavioral state operating at multiple neuronal levels through the activities of a kinase and a phosphatase. These results in a genetically tractable organism establish a framework for further dissection of the mechanism of quiescence during episodic behaviors.
Highlights
Most rhythmic motor behaviors in nature are episodic i.e. they alternate between different behavioral states, including quiescence
protein kinase G (PKG) is required for maintenance of the quiescent state during swimming in liquid The PKG homolog of C. elegans, egl-4, regulates longterm olfactory adaptation [15], different locomotory states [16] and promotes longer duration of quiescence bouts under different paradigms [11,12,13]
Though it is widely expressed in the neuromuscular system and has been implicated in modulation of acetylcholine release at neuromuscular junctions [17], the pleiotropic effects of egl-4 have been mostly attributed to its activity in sensory neurons [15,16,17,18]
Summary
Most rhythmic motor behaviors in nature are episodic i.e. they alternate between different behavioral states, including quiescence. Electrophysiological studies in invertebrate behavioral switching, maintenance and quiescence have elucidated several neuronal mechanisms that generate a temporal pattern in behavior. We have previously uncovered a novel episodic behavior exhibited by C. elegans in liquid media where they alternate between distinct phases of rhythmic swimming and quiescence. Invertebrate electrophysiological studies of a given behavioral state such as quiescence and switching between behavioral states e.g. swimming and crawling in Tritonia [3,4], swallowing and quiescent states in Lymnea [5] among many others have elucidated several neuronal mechanisms. Despite a single gait underlying locomotion in liquid and solid media [6], referred to as swimming [7,8] and crawling respectively, nematodes exhibit distinct behavioral patterns when observed for long periods of time in liquid [9,10]. We previously showed that quiescence in liquid results from high cholinergic signaling downstream of motor neurons and that the maintenance of the quiescent state requires command inter-neurons [9]
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