Long-Lasting Activation of Rhythmic Neuronal Activity by a Novel Mechanosensory System in the Crustacean Stomatogastric Nervous System

Abstract

Sensory neurons enable neural circuits to generate behaviors appropriate for the current environmental situation. Here, we characterize the actions of a population (about 60) of bilaterally symmetric bipolar neurons identified within the inner wall of the cardiac gutter, a foregut structure in the crab Cancer borealis. These neurons, called the ventral cardiac neurons (VCNs), project their axons through the crab stomatogastric nervous system to influence neural circuits associated with feeding. Brief pressure application to the cardiac gutter transiently modulated the filtering motor pattern (pyloric rhythm) generated by the pyloric circuit within the stomatogastric ganglion (STG). This modulation included an increased speed of the pyloric rhythm and a concomitant decrease in the activity of the lateral pyloric neuron. Furthermore, 2 min of rhythmic pressure application to the cardiac gutter elicited a chewing motor pattern (gastric mill rhythm) generated by the gastric mill circuit in the STG that persisted for < or =30 min. These sensory actions on the pyloric and gastric mill circuits were mimicked by either ventral cardiac nerve or dorsal posterior esophageal nerve stimulation. VCN actions on the STG circuits required the activation of projection neurons in the commissural ganglia. A subset of the VCN actions on these projection neurons appeared to be direct and cholinergic. We propose that the VCN neurons are mechanoreceptors that are activated when food stored in the foregut applies an outward force, leading to the long-lasting activation of projection neurons required to initiate chewing and modify the filtering of chewed food.

Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

“…1 A), so the influence of this projection neuron on the gastric mill circuit was eliminated readily by transecting this nerve. Although one other projection neuron (MCN5) (Coleman et al, 1992;Norris et al, 1996) also takes this route to the STG and thus is eliminated with ion nerve transection, the activity level of MCN5 after VCN stimulation is too low to have an impact on the gastric mill rhythm (Norris et al, 1996;Beenhakker et al, 2004). Nonetheless, because of the presence of MCN5 in the ion, we were motivated to determine whether MCN1 and CPN2 activity was sufficient to recapitulate the VCN-elicited gastric mill rhythm (see below and Results).…”

“…The actions of several sensory systems on the STG circuits have been documented (Simmers and Moulins, 1988a,b;Katz et al, 1989;Hooper et al, 1990;Meyrand et al, 1994;Combes et al, 1999a;Beenhakker et al, 2004). One of these systems, the ventral cardiac neuron (VCN) mechanosensory system, is a population of sensory neurons innervating the wall of the cardiac sac stomach compartment that are hypothesized to detect foregut distention .…”

“…It is already evident that there are multiple versions of the gastric mill rhythm Norris et al, 1994;Beenhakker et al, 2004). However, to demonstrate that the gastric mill circuit is truly under the control of a code that is represented by overlapping but distinct populations of upstream projection neurons, the actions of several different sensory systems on those projection neurons, as well as the consequences of such actions for the gastric mill circuit, must be examined next.…”

Muscles innervated by a single motor neuron exhibit divergent synaptic properties on multiple time scales

“…The single firing rate (10 Hz=100 ms inter-spike interval) and burst duration (4.8 s) used were also within the physiological range of LG activity (inter-spike interval: 50-250 ms; burst duration: 2-9 s) (Beenhakker et al, 2004(Beenhakker et al, , 2005(Beenhakker et al, , 2007Blitz et al, 2004bBlitz et al, , 2008Colton and Nusbaum, 2014;DeLong and Nusbaum, 2010;Diehl et al, 2013;Hedrich et al, 2011;Kirby and Nusbaum, 2007;White and Nusbaum, 2011). Thus, our data indicate that during gastric mill rhythms triggered by multiple inputs, augmentation and facilitation/ depression would regulate responses of the three target muscles of LG.…”

“…Diehl et al (2013) focused on distinctions in the pattern of spiking within LG bursts, but a number of other aspects of LG activity differ depending on modulatory state and the complement of inputs acting on LG. In response to a number of different modulatory inputs, LG activity consists of firing rates of 4-20 Hz (50-250 ms inter-spike intervals), burst durations of 2-8 s and interburst intervals of 2-24 s in vitro and in vivo (Beenhakker et al, 2004(Beenhakker et al, , 2005(Beenhakker et al, , 2007Blitz et al, 2004bBlitz et al, , 2008Colton and Nusbaum, 2014;DeLong and Nusbaum, 2010;Diehl et al, 2013;Hedrich et al, 2011;Kirby and Nusbaum, 2007;White and Nusbaum, 2011). Similar to central and peripheral synapses in other systems, electrical responses at neuromuscular junctions in the STNS are shaped by multiple forms of activity-dependent synaptic plasticity including depression, facilitation and augmentation (Daur et al, 2012b;Jorge-Rivera et al, 1998;Katz et al, 1993;Sen et al, 1996;Stein et al, 2006).…”