Coupling between fast and slow oscillator circuits in Cancer borealis is temperature-compensated.

Daniel Powell,Sara A Haddad,Eve Marder,Srinivas Gorur-Shandilya

doi:10.7554/elife.60454

Abstract

Coupled oscillatory circuits are ubiquitous in nervous systems. Given that most biological processes are temperature-sensitive, it is remarkable that the neuronal circuits of poikilothermic animals can maintain coupling across a wide range of temperatures. Within the stomatogastric ganglion (STG) of the crab, Cancer borealis, the fast pyloric rhythm (~1 Hz) and the slow gastric mill rhythm (~0.1 Hz) are precisely coordinated at ~11°C such that there is an integer number of pyloric cycles per gastric mill cycle (integer coupling). Upon increasing temperature from 7°C to 23°C, both oscillators showed similar temperature-dependent increases in cycle frequency, and integer coupling between the circuits was conserved. Thus, although both rhythms show temperature-dependent changes in rhythm frequency, the processes that couple these circuits maintain their coordination over a wide range of temperatures. Such robustness to temperature changes could be part of a toolbox of processes that enables neural circuits to maintain function despite global perturbations.

Highlights

Coupled oscillators are common in nervous systems
The gastric mill rhythm can be evoked by stimulating projection neurons found within the commissural ganglia (CoGs), and has a characteristic period of 6-10 sec (Beenhakker et al, 2004)
These recordings show alternating bursts of activity in the Lateral Gastric (LG) and Dorsal Gastric (DG) neurons, with the Gastric Mill (GM) neurons firing at the end of the LG burst

Summary

Introduction

Oscillatory circuits may have distinct frequencies and duty cycles, coordination between them is often necessary for proper function (Nadim et al, 1998; Bartos et al, 1999; Colgin, 2011; Gordon, 2011; Jacobson et al, 2013; Rojas-Líbano et al, 2014; Harris and Gordon, 2015; Karalis et al, 2016; Tamura et al, 2017). Theta frequency circuits coupled to those in the gamma range are thought to drive both sensory and behavioral processing (Lisman and Buzsáki, 2008; Fujisawa and Buzsáki, 2011; Gordon, 2011; Lisman and Jensen, 2013). The coordination of oscillatory circuits, often with distinct temporal features, is key to circuit function and information processing. Because fluctuations in a circuit’s environment can impact function (Fonseca and Correia, 2007; Tang et al, 2010; Haddad and Marder, 2018; Haley et al, 2018; Kushinsky et al, 2019; He et al, 2020), it is important to know how robust this coordination is to externally or internally generated perturbations

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