Regulation of motor patterns by the central spike‐initiation zone of a sensory neuron

Abstract

Sensory feedback from muscles and peripheral sensors acts to initiate, tune or reshape motor activity according to the state of the body. Yet, sensory neurons often show low levels of activity even in the absence of sensory input. Here we examine the functional role of spontaneous low-frequency activity of such a sensory neuron. The anterior gastric receptor (AGR) is a muscle tendon organ in the crab stomatogastric nervous system whose phasic activity shapes the well-characterized gastric mill (chewing) and pyloric (filtering) motor rhythms. Phasic activity is driven by a spike initiation zone near the innervated muscle. We here demonstrate that AGR possesses a second spike initiation zone, which is located spatially distant from the innervated muscle in a central section of the axon. This initiation zone generates tonic activity and is responsible for the spontaneous activity of AGR in vivo, but does not code sensory information. Rather, it is sensitive to the neuromodulator octopamine. A computational model indicates that the activity at this initiation zone is not caused by excitatory input from another neuron, but generated intrinsically. This tonic activity is functionally relevant, because it modifies the activity state of the gastric mill motor circuit and changes the pyloric rhythm. The sensory function of AGR is not impaired since phasic activity suppresses spiking at the central initiation zone. Our results thus demonstrate that sensory neurons are not mere reporters of sensory signals. Neuromodulators can elicit non-sensory coding activity in these neurons that shapes the state of the motor system.

Optical Imaging of Neuronal Activity and Visualization of Fine Neural Structures in Non-Desheathed Nervous Systems

“…Our findings support the conclusion of Daur et al [23] in that axonal modulation not only occurs spontaneously, but is reliably present when gastric mill rhythms are elicited. While changes in AGR firing frequency had been observed, they had never been correlated to the motor pattern before.…”

Hidden synaptic differences in a neural circuit underlie differential behavioral susceptibility to a neural injury

“…Perhaps a discussion in that context would be useful (e.g. Daur, Nadim and Stein, 2009 . European Journal of Neuroscience, Vol.…”

Restoration of descending inputs fails to rescue activity following deafferentation of a motor network

“…It begins to fire two independent spikes (instead of a single, tonic spike), one of which propagates through the son, stn, and dgn that appears to originate in the stn, whereas a second independent spike propagates only in the dgn in our recordings (Fig. 5, 72-h block, far right; see also Daur et al 2009). …”

“…These effects do not seem to simply be due to damage of the descending stn fibers. Using AGR activity as a monitor of stn propagation ability (Daur et al 2009), we found no significant differences in AGR spike propagation ability over time in both control and sucrose preparations, indicating the propagation ability of the stn is likely maintained throughout these experiments.…”

“…In addition to blocking descending fibers, the blockade may also influence any ascending feedback from the STG to the commissural ganglia, as represented in our studies by AGR activity (Daur et al 2009). In this study we consider both possibilities, but do not distinguish between the two.…”