Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

Abstract

Sensorimotor gating commonly occurs at sensory neuron synapses onto motor circuit neurons and motor neurons. Here, using the crab stomatogastric nervous system, we show that sensorimotor gating also occurs at the level of the projection neurons that activate motor circuits. We compared the influence of the gastro-pyloric receptor (GPR) muscle stretch-sensitive neuron on two projection neurons, modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2 (CPN2), with and without a preceding activation of the mechanosensory ventral cardiac neurons (VCNs). MCN1 and CPN2 project from the paired commissural ganglia (CoGs) to the stomatogastric ganglion (STG), where they activate the gastric mill (chewing) motor circuit. When stimulated separately, the GPR and VCN neurons each elicit the gastric mill rhythm by coactivating MCN1 and CPN2. When GPR is instead stimulated during the VCN-gastric mill rhythm, it slows this rhythm. This effect results from a second GPR synapse onto MCN1 that presynaptically inhibits its STG terminals. Here, we show that, during the VCN-triggered rhythm, the GPR excitation of MCN1 and CPN2 in the CoGs is gated out, leaving only its influence in the STG. This gating effect appears to occur within the CoG and does not result from a ceiling effect on projection neuron firing frequency. Additionally, this gating action enables GPR to either activate rhythmic motor activity or act as a phasic sensorimotor feedback system. These results also indicate that the site of sensorimotor gating can occur at the level of the projection neurons that activate a motor circuit.

Multiple Mechanisms for Integrating Proprioceptive Inputs That Converge on the Same Motor Pattern-Generating Network

“…To address this issue, we used the lobster stomatogastric nervous system, which has already been extensively described in terms of identified proprioceptive inputs (Simmers and Moulins, 1988a;Katz et al, 1989;Combes et al, 1995;Beenhakker et al, 2004Beenhakker et al, , 2007, their interneuronal projection pathways, and target motor circuitry (Harris-Warrick and Marder and Calabrese, 1996;Combes et al, 1999a,b;Nusbaum and Beenhakker, 2002;. Here, we show that sensory input from one proprioceptor, the PSR, modifies the influence on the gastric mill network of another mechanoreceptor, AGR, via a combination of convergent postsynaptic actions on common projection interneurons and presynaptic interactions between two afferent pathways themselves.…”

“…Inputs from joint receptors (Lundberg et al, 1978) and spindle afferents (Jankowska and McCrea, 1983) also influence tension regulation from Golgi tendon organs, again through convergence at the premotoneuronal level. In locust, mechanosensory afferents from different leg exteroceptors make central connections with the same local interneurons (Burrows and Newland, 1994), and in the stomatogastric system of crabs, mechanoreceptors other than PSR and AGR also have access to motor circuitry via common projection neurons Beenhakker et al, 2007).…”

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).…”

Serotonin Transduction Cascades Mediate Variable Changes in Pyloric Network Cycle Frequency in Response to the Same Modulatory Challenge

“…This apparent discrepancy is easily explained for work examining modulation by projection neurons onto circuit neurons (e.g., Saideman et al 2007a;Stein et al 2007) and/or extrinsic inputs onto these projection neurons (e.g., Beenhakker et al 2007;Blitz et al 2008). Since these types of studies usually use an intact preparation (i.e., nondeafferented), it may be that reproducibility is maintained through stabilizing mechanisms involving additional modulatory inputs and/or feedback from STG neurons to input neurons Coleman et al 1995;Wood et al 2004).…”