Abstract

We investigated the central nervous coordination between singing motor activity and abdominal ventilatory pumping in crickets. Fictive singing, with sensory feedback removed, was elicited by eserine-microinjection into the brain, and the motor activity underlying singing and abdominal ventilation was recorded with extracellular electrodes. During singing, expiratory abdominal muscle activity is tightly phase coupled to the chirping pattern. Occasional temporary desynchronization of the two motor patterns indicate discrete central pattern generator (CPG) networks that can operate independently. Intracellular recordings revealed a sub-threshold depolarization in phase with the ventilatory cycle in a singing-CPG interneuron, and in a ventilation-CPG interneuron an excitatory input in phase with each syllable of the chirps. Inhibitory synaptic inputs coupled to the syllables of the singing motor pattern were present in another ventilatory interneuron, which is not part of the ventilation-CPG. Our recordings suggest that the two centrally generated motor patterns are coordinated by reciprocal feedforward discharges from the singing-CPG to the ventilation-CPG and vice versa. Consequently, expiratory contraction of the abdomen usually occurs in phase with the chirps and ventilation accelerates during singing due to entrainment by the faster chirp cycle.

Highlights

  • In all animals the timing of rhythmic muscle activity during simultaneous repetitive motor behaviors is well coordinated

  • In the stomatogastric system of crustaceans the rhythmic synaptic input from the pyloric central pattern generator (CPG) can modulate the activity of the gastric mill CPG (Nadim et al 1998; Bartos et al 1999; Nusbaum and Beenhakker 2002), in the crayfish abdominal swimmeret system gradients of synaptic strength underlie the coordination of swimmerets (Smarandache et al 2009), and evidence points to local CPGs being weakly coupled to support inter-leg coordination in walking insects (Knebel et al 2016; Bidaye et al 2017; Daun et al 2019)

  • We investigated the neural coordination between the motor patterns of abdominal ventilation and the generation of chirps in fictively singing field crickets (Gryllus bimaculatus de Geer)

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Summary

Introduction

In all animals the timing of rhythmic muscle activity during simultaneous repetitive motor behaviors is well coordinated (von Holst 1935, 1943; Kutsch 1969; Syed and Winlow 1991; Dick et al 1993; Chrachri and Neil 1993; Ramirez 1998; Boggs 2002; Moore et al 2014; Stein 2018). The rhythm generating network for ventilation in orthopteran insects is located in the metathoracic and subsequent abdominal ganglia (Huber 1960; Miller 1960, 1966; Lewis et al 1973; Ramirez and Pearson 1989a; Burrows 1996; Bustami and Hustert 2000) which in crickets is the same part of the central nervous system that houses the singing-CPG for the calling song (Hennig and Otto 1995; Schöneich and Hedwig 2011, 2012, 2017; Jacob and Hedwig 2016, 2019). In crickets abdominal ventilation and singing are suited behaviors to unravel the neuronal basis of central motor pattern coordination

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