State-Dependent Presynaptic Inhibition Regulates Central Pattern Generator Feedback to Descending Inputs

Abstract

Central pattern generators (CPGs) provide feedback to their projection neuron inputs. However, it is unknown whether this feedback is regulated and how that might shape CPG output. We are studying feedback from the pyloric CPG to identified projection neurons that regulate the gastric mill CPG, in the crab stomatogastric nervous system. Both CPGs are located in the stomatogastric ganglion (STG) and are influenced by projection neurons originating in the paired commissural ganglia (CoGs). Two extrinsic inputs [ventral cardiac neurons (VCNs) and postoesophageal commissure (POC) neurons] trigger distinct gastric mill rhythms despite acting via the same projection neurons [modulatory commissural neuron 1 (MCN1); commissural projection neuron 2 (CPN2)]. These projection neurons receive feedback inhibition from the pyloric CPG interneuron anterior burster (AB), resulting in their exhibiting pyloric-timed activity during the retraction phase of the VCN- and POC-triggered gastric mill rhythms. However, during the gastric mill protraction phase, MCN1/CPN2 exhibit pyloric-timed activity during the POC-triggered rhythm but fire tonically during the VCN-triggered rhythm. Here, we show that the latter, tonic activity pattern results from the elimination of AB inhibition of MCN1/CPN2, despite persistent AB actions within the STG and AB action potentials still propagating into each CoG. This loss of pyloric-timed AB input likely results from presynaptic inhibition of AB in each CoG because, when a secondary rhythmic AB burst initiation zone in the CoG is activated, the associated action potentials are selectively suppressed during the VCN protraction phase. Thus, rhythmic CPG feedback can be locally regulated, in a state-dependent manner, enabling the same projection neurons to drive multiple motor patterns from the same neuronal circuit.