Abstract
Neuropeptides play a key role in the regulation of behaviors and physiological responses including alertness, social recognition, and hunger, yet, their mechanism of action is poorly understood. Here, we focus on the endocrine control ecdysis behavior, which is used by arthropods to shed their cuticle at the end of every molt. Ecdysis is triggered by ETH (Ecdysis triggering hormone), and we show that the response of peptidergic neurons that produce CCAP (crustacean cardioactive peptide), which are key targets of ETH and control the onset of ecdysis behavior, depends fundamentally on the actions of neuropeptides produced by other direct targets of ETH and released in a broad paracrine manner within the CNS; by autocrine influences from the CCAP neurons themselves; and by inhibitory actions mediated by GABA. Our findings provide insights into how this critical insect behavior is controlled and general principles for understanding how neuropeptides organize neuronal activity and behaviors.
Highlights
Understanding how ensembles of neurons produce behaviors is an important aim of neuroscience
Consistent with the behaviors observed at ecdysis, the pattern of motor activity expressed in vitro in response to ecdysis-triggering hormone (ETH) consists of an initial phase that primarily recruits activity in the posterior region of the ventral nervous system (VNS) (’P’ region, Figure 1Ab, Ba; corresponding to pre-ecdysis) followed by a barrage of activity throughout the left and right sides of the VNS neuropils (’L’, Figure 1Ac; Bb; and ’R’ regions, Figure 1Ad; Bd)
The Crustacean Cardioactive Peptide (CCAP) neurons express ETH receptor (ETHR), and by targeting ETHR RNAi to these neurons we showed that the timecourse and intensity of their response to ETH is sensitive to the dosage of ETHR
Summary
Understanding how ensembles of neurons produce behaviors is an important aim of neuroscience. The mapping of the neural circuits that underlie a behavior is considered a necessary first step toward this goal, and efforts to determine the ‘connectome’ of different parts of the nervous system have been present since the beginnings of modern neuroscience They start with the classical inferred synaptic relationships in Cajal’s anatomical analyses (Ramon y Cajal, 1899), through the detailed information on the wiring of some invertebrate circuits (e.g., Carew et al, 1981; Comer and Robertson, 2001; King, 1976a, 1976b), culminating with the complete map of the Caenorhabditis elegans central nervous system (CNS) (White et al, 1986), and the wiring diagrams of the Drosophila optic lobes (Takemura et al, 2013) and the mammalian retina (Helmstaedter et al, 2013). In conjunction with classical transmitters, they can gate the input to a circuit or reconfigure its pattern of activity, thereby causing the same circuit to produce qualitatively different outputs (Bargmann, 2012; Bargmann and Marder, 2013; Brezina, 2010; Leinwand and Chalasani, 2013; Marder, 2012; Nusbaum and Blitz, 2012)
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