Neuropeptide modulation of pattern-generating systems in crustaceans: comparative studies and approaches

Abstract

Central pattern generators are subject to modulation by peptides, allowing for flexibility in patterned output. Current techniques used to characterize peptides include mass spectrometry and transcriptomics. In recent years, hundreds of neuropeptides have been sequenced from crustaceans; mass spectrometry has been used to identify peptides and to determine their levels and locations, setting the stage for comparative studies investigating the physiological roles of peptides. Such studies suggest that there is some evolutionary conservation of function, but also divergence of function even within a species. With current baseline data, it should be possible to begin using comparative approaches to ask fundamental questions about why peptides are encoded the way that they are and how this affects nervous system function.

AMGSEFLamide, a member of a broadly conserved peptide family, modulates multiple neural networks inHomarus americanus

“…locomotion), is often imparted by the physiological effects of circulating neurohormones and/or locally released neuromodulators, the largest class of which is peptides (e.g. Dickinson et al, 2016;Nusbaum and Blitz, 2012;Nusbaum et al, 2017;Taghert and Nitabach, 2012). Recent advances in genomics/transcriptomics have enabled the identification of many new peptides in a variety of animals, including crustaceans (e.g.…”

“…The present study is a multi-faceted examination of the GSEFLamide family, with a primary focus on the American lobster, Homarus americanus, a model species for investigating the modulation of rhythmic motor behaviours (e.g. Christie, 2011;Christie et al, 2010b;Dickinson et al, 2016;Nusbaum and Blitz, 2012;Nusbaum et al, 2017;Stein, 2009). Several transcriptomes (Christie et al, 2015(Christie et al, , 2018cNorthcutt et al, 2016), including one specific for the eyestalk ganglia (Christie et al, 2017b), which is the locus of the neuroendocrine X-organ-sinus-gland (XO-SG) complex (e.g.…”

New techniques, applications and perspectives in neuropeptide research

“…In terms of neurological studies, in vitro whole-cell recordings are the most common, although in vivo live-animal recordings, which are inherently more difficult, are becoming more refined (Scanziani and Häusser, 2009). Crustacean model systems have been used heavily for electrophysiological studies (Daur et al, 2016;Dickinson et al, 2016;Otopalik et al, 2017). For example, the effects of neuromodulators on the same neuronal circuit was explored for the Jonah crab gastric mill motor pattern, which was interestingly explained by using a mathematical model (Kintos et al, 2016).…”

Molecular characterization of putative neuropeptide, amine, diffusible gas and small molecule transmitter biosynthetic enzymes in the eyestalk ganglia of the American lobster, Homarus americanus

“…Due to their numerical simplicity and the large size of their component neurons, the cardiac and stomatogastric nervous systems of decapod crustaceans, including those of the lobster H. americanus, are arguably the best understood rhythmically active neural circuits. As such, these neural networks have long served as models for investigating the basic principles underlying the generation, maintenance and modulation of rhythmically active motor behavior generally (e.g., Blitz and Nusbaum, 2011;Christie et al, 2010;Cooke, 2002;Dickinson et al, 2016;Fénelon et al, 2003;Harris-Warrick et al, 1992;Hooper and DiCaprio, Marder and Bucher, 2007;Marder et al, 1995;Nusbaum et al, 2001;Selverston, 2005;Selverston and Ayers, 2006;Selverston and Moulins, 1987;Selverston et al, 1998;Skiebe, 2001;Stein, 2009), including walking, chewing and breathing in humans. A key finding made using the cardiac and stomatogastric systems is that "hard-wired" neural networks, even very simple ones, can produce an almost infinite array of motor outputs via the actions of locally-released and circulating neuromodulators/neurotransmitters, including peptides, amines, diffusible gases and small molecule transmitters.…”

“…Due to its culinary notoriety, the American lobster, Homarus americanus, is one of the world's most well-known crustaceans; portions of its nervous system, specifically the cardiac ganglion and the stomatogastric nervous system, are also well-established biomedical models that have contributed greatly to our understanding of the basic principles underlying the generation, maintenance and modulation of rhythmically active motor behaviors across the animal kingdom (e.g., Blitz and Nusbaum, 2011;Christie et al, 2010;Cooke, 2002;Dickinson et al, 2016;Fénelon et al, 2003;Harris-Warrick et al, 1992;Hooper and DiCaprio, Marder and Bucher, 2007;Marder et al, 1995;Nusbaum et al, 2001;Selverston, 2005;Selverston and Ayers, 2006;Selverston and Moulins, 1987;Selverston et al, 1998;Skiebe, 2001;Stein, 2009). One finding derived from studies conducted on the central pattern generator-effector systems of H. americanus and other decapod species is that numerically simple, "hard-wired" neural networks can produce an extensive array of distinct motor outputs via the actions of locally-released and circulating chemical compounds that act to modify the intrinsic properties of the neurons that form these circuits.…”