Proprioceptor Regulation of Motor Circuit Activity by Presynaptic Inhibition of a Modulatory Projection Neuron

Abstract

Phasically active sensory systems commonly influence rhythmic motor activity via synaptic actions on the relevant circuit and/or motor neurons. Using the crab stomatogastric nervous system (STNS), we identified a distinct synaptic action by which an identified proprioceptor, the gastropyloricmusclestretchreceptor(GPR)neuron,regulatesthegastricmill(chewing)motorrhythm.Previousworkshowedthatrhythmically stimulating GPR in a gastric mill-like pattern, in the isolated STNS, elicits the gastric mill rhythm via its activation of two identified projection neurons, modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2, in the commissural ganglia. Here, we determine how activation of GPR with a behaviorally appropriate pattern (active during each gastric mill retractor phase) influences an ongoing gastric mill rhythm via actions in the stomatogastric ganglion, where the gastric mill circuit is located. Stimulating GPR during each retractor phase selectively prolongs that phase and thereby slows the ongoing rhythm. This selective action on the retractor phase results from two distinct GPR actions. First, GPR presynaptically inhibits the axon terminals of MCN1, reducing MCN1 excitation of all gastric mill neurons. Second, GPR directly excites the retractor phase neurons. Because MCN1 transmitter release occurs during each retractor phase, these parallel GPR actions selectively reduce the buildup of excitatory drive to the protractor phase neurons, delaying each protractor burst. Thus, rhythmic proprioceptor feedback to a motor circuit can result from a global reduction in excitatory drive to that circuit, via presynaptic inhibition, coupled with a phase-specific excitatory input that prolongs the excited phase by delaying the onset of the subsequent phase.

Convergent Motor Patterns from Divergent Circuits

“…Thus, when the pyloric rhythm was suppressed the Int1 inhibition of LG was constant, as well as stronger than PK excitation, which maintained LG at a hyperpolarized potential and prevented postinhibitory rebound bursts. In contrast, the continual buildup of MCN1 excitation enables LG to escape from Int1-mediated inhibition and fire an impulse burst when AB activity is suppressed (Bartos et al, 1999;Beenhakker et al, 2005). However, during the MCN1 rhythm with an ongoing pyloric rhythm, each LG burst initiates during an episode of AB inhibition of Int1, suggesting that escape from inhibition and postinhibitory rebound both contribute to LG burst onset during this rhythm (Bartos et al, 1999).…”

“…These different rhythms result mainly from differences in the MCN1 activity pattern and/or firing rate, and the level of participation of a second projection neuron, commissural projection neuron 2. In all of these rhythms, the core CPG includes the reciprocally inhibitory STG neurons LG and Int1 plus the STG terminals of MCN1 Bartos et al, 1999;Wood et al, 2004;Beenhakker et al, 2005). MCN1 is considered to be a gastric mill CPG neuron as well as a rhythm activator because it must release its cotransmitter complement in a gastric mill rhythm-timed pattern to drive this rhythm .…”

“…Additional distinctions between the PK-and MCN1-elicited gastric mill rhythms are likely to be identified, particularly those involving pathways that act via MCN1 and/or the DG neuron. For example, the GPR proprioceptor regulates the gastric mill rhythm by presynaptically inhibiting the STG terminals of MCN1 (Beenhakker et al, 2005). Whatever the influence of GPR on the PK-elicited rhythm, it cannot occur via MCN1.…”

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

“…D, Stimulating GPR at the behaviorally appropriate time slows the VCN-elicited gastric mill rhythm by prolonging the retractor phase. Rhythmic stimulation of GPR (bars, 5 Hz) during the retractor phase (DG neuron active) of a VCN-triggered gastric mill rhythm caused a progressively increasing prolongation of the retractor phase (Beenhakker et al, 2005).…”

“…Despite activating the gastric mill rhythm by targeting the same projection neurons, the GPR-elicited rhythm is slower and shorter-lasting than the one triggered by VCN stimulation . Stimulating GPR during the VCNtriggered gastric mill rhythm slows this rhythm as well by selectively prolonging the gastric mill retractor phase, at least partly via GPR inhibition of the STG terminals of MCN1 (MCN1 STG ) (Beenhakker et al, 2005).…”