Sources and range of long-term variability of rhythmic motor patternsin vivo.

Abstract

The mechanisms of rhythmic motor pattern generation have been studied in detail in vitro, but the long-term stability and sources of variability in vivo are often not well described. The crab stomatogastric ganglion contains the well-characterized gastric mill (chewing) and pyloric (filtering of food) central pattern generators. In vitro, the pyloric rhythm is stereotyped with little variation, but intercircuit interactions and neuromodulation can alter both rhythm cycle frequency and structure. The range of variation of activity in vivo is, with few exceptions, unknown. Curiously, although the patterngenerating circuits in vivo are constantly exposed to hormonal and neural modulation, the majority of published data show only the unperturbed canonical motor patterns typically observed in vitro. Using long-term extracellular recordings (N=27 animals), we identified the range and sources of variability of the pyloric and gastric mill rhythms recorded continuously over 4 days in freely behaving Jonah crabs (Cancer borealis). Although there was no evidence of innate daily rhythmicity, a 12 h light-driven cycle did manifest. The frequency of both rhythms increased modestly, albeit consistently, during the 3 h before and 3 h after the lights changed. This cycle was occluded by sensory stimulation (feeding), which significantly influenced both pyloric cycle frequency and structure. This was the only instance where the structure of the rhythm changed. In unfed animals the structure remained stable, even when the frequency varied substantially. So, although central pattern generating circuits are capable of producing many patterns, in vivo outputs typically remain stable in the absence of sensory stimulation.

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

“…Like the neural circuit in the CG, the pyloric network in the STG is constitutively active in intact animals (e.g. Clemens et al, 1998a, b;Harris-Warrick et al, 1992;Rezer and Moulins, 1983;Selverston and Moulins, 1987;Yarger and Stein, 2015); it is also virtually always active in the isolated STNS when the stn, which carries inputs from the more anterior ganglia (CoGs and OG) to the STG, is intact (e.g. Harris-Warrick et al, 1992;Selverston and Moulins, 1987).…”

Output variability across animals and levels in a motor system

“…In zebrafish literature again episodes and animals are convolved making it difficult to parse repetition variance and population variance ( Masino and Fetcho, 2005 ; Wiggin et al, 2014 ). The heroic enterprise to record from several motor neurons in the STNS in vivo over several days ( Yarger and Stein, 2015 ) does not tease apart the phase variability across episodes and across animals for the episodic gastric motor pattern.…”

“…But how constant is network output across individuals? Not very seems to be the answer when looking at the literature more closely (e.g., locomotion in mice [ Bellardita and Kiehn, 2015 ] and zebrafish [ Masino and Fetcho, 2005 ; Wiggin et al, 2014 ]; food processing in crabs [ Hamood et al, 2015 ; Hamood and Marder, 2015 ; Yarger and Stein, 2015 ], crawling in fly larvae [ Pulver et al, 2015 ]).…”

Long-Distance Modulation of Sensory Encoding via Axonal Neuromodulation

“…The STG is subject to heavy neuromodulation from hormones in the blood stream and from peptide and amine modulators released from descending modulatory projection neurons [44][45][46]. In vitro, modulation is reduced, potentially leading to a much reduced variability in activity in comparison to in vivo [47]. The reduced modulation may account for the smaller range of AGR frequencies when compared to intact animals.…”