Abstract
Cell- or network-driven oscillators underlie motor rhythmicity. The identity of C. elegans oscillators remains unknown. Through cell ablation, electrophysiology, and calcium imaging, we show: (1) forward and backward locomotion is driven by different oscillators; (2) the cholinergic and excitatory A-class motor neurons exhibit intrinsic and oscillatory activity that is sufficient to drive backward locomotion in the absence of premotor interneurons; (3) the UNC-2 P/Q/N high-voltage-activated calcium current underlies A motor neuron's oscillation; (4) descending premotor interneurons AVA, via an evolutionarily conserved, mixed gap junction and chemical synapse configuration, exert state-dependent inhibition and potentiation of A motor neuron's intrinsic activity to regulate backward locomotion. Thus, motor neurons themselves derive rhythms, which are dually regulated by the descending interneurons to control the reversal motor state. These and previous findings exemplify compression: essential circuit properties are conserved but executed by fewer numbers and layers of neurons in a small locomotor network.
Highlights
Central pattern generators (CPGs) are rhythm-generating neurons and neural circuits with self-sustained oscillatory activities
To address whether and where CPGs are present, we first examined the behavioral consequence of systematic ablation of motor neurons (MNs) and premotor INs
388 We show that distinct locomotor CPGs underlie C. elegans forward and reversal movements
Summary
Central pattern generators (CPGs) are rhythm-generating neurons and neural circuits with self-sustained oscillatory activities. Isolated spinal or nerve cords from the leech (Briggman and Kristan, 2006), lamprey (Wallen and Williams, 1984), rat (Juvin et al, 2007; Kiehn et al, 1992), and cat (Guertin et al, 1995) were capable of generating rhythmic MN activity and/or fictive locomotion. These findings suggest that locomotor systems intrinsically sustain rhythmic and patterned electric activity, independent of inputs from the descending neural networks or sensory organs
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