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

Abstract

Adaptive changes in the output of neural circuits underlying rhythmic behaviors are relayed to muscles via motor neuron activity. Presynaptic and postsynaptic properties of neuromuscular junctions can impact the transformation from motor neuron activity to muscle response. Further, synaptic plasticity occurring on the time scale of inter-spike intervals can differ between multiple muscles innervated by the same motor neuron. In rhythmic behaviors, motor neuron bursts can elicit additional synaptic plasticity. However, it is unknown whether plasticity regulated by the longer time scale of inter-burst intervals also differs between synapses from the same neuron, and whether any such distinctions occur across a physiological activity range. To address these issues, we measured electrical responses in muscles innervated by a chewing circuit neuron, the lateral gastric (LG) motor neuron, in a well-characterized small motor system, the stomatogastric nervous system (STNS) of the Jonah crab, Cancer borealis. In vitro and in vivo, sensory, hormonal and modulatory inputs elicit LG bursting consisting of inter-spike intervals of 50-250 ms and inter-burst intervals of 2-24 s. Muscles expressed similar facilitation measured with paired stimuli except at the shortest interspike interval. However, distinct decay time constants resulted in differences in temporal summation. In response to bursting activity, augmentation occurred to different extents and saturated at different inter-burst intervals. Further, augmentation interacted with facilitation, resulting in distinct intra-burst facilitation between muscles. Thus, responses of multiple target muscles diverge across a physiological activity range as a result of distinct synaptic properties sensitive to multiple time scales.

Synaptic Dynamics Convey Differential Sensitivity to Input Pattern Changes in Two Muscles Innervated by the Same Motor Neurons

“…Both cpv2a and cpv2b showed response dynamics dominated by facilitation, as is typical for stomach muscles (Govind and Lingle, 1987;Jorge-Rivera et al, 1998;Stein et al, 2006;Blitz et al, 2017). Apart from occasional GAPs, unitary EJPs waveforms, temporal summation, and facilitation in cpv2a were similar to synaptic responses in other pyloric muscles (Govind et al, 1975;Govind and Lingle, 1987;Pulver et al, 2005;Daur et al, 2012).…”

“…Slower forms of synaptic plasticity like augmentation, post-tetanic potentiation, and long-lasting depression are only apparent with longer lasting and highly repetitive synaptic activation and can depend on a range of cellular phenomena (Regehr and Stevens, 2001;Zucker and Regehr, 2002). Pyloric neuron activity is highly repetitive, and the time constants of recovery from facilitation shown in Figure 4 suggested that dynamics could extend over multiple burst inputs, as has been shown for other stomach muscles (Stein et al, 2006;Blitz et al, 2017). We did not attempt to distinguish between cellular mechanisms that may be involved in dynamics apparent at different timescales, either pre-or postsynaptically.…”

“…Crustacean stomach NMJs show substantial short-term synaptic plasticity, in most cases facilitation (Govind and Lingle, 1987;Sen et al, 1996;Jorge-Rivera et al, 1998;Stein et al, 2006;Daur et al, 2012;Blitz et al, 2017). To explore the dynamics of EJP responses, we used electrical stimulation of the pdn to activate PD axons in different patterns.…”

“…In one case, one NMJ showed facilitation and the other depression (Katz et al, 1993). In other cases, NMJs all facilitated, but magnitude and frequency-dependence varied (Govind et al, 1975;Blitz et al, 2017). Such differences have not been systematically explored in the context of sensitivity to different attributes of neuron and circuit activity in the stomatogastric system.…”

“…The functional significance of such changes for muscle activation are not well understood. Neuromuscular junctions (NMJs) at the striated stomatogastric muscles show diverse synaptic dynamics (Jorge-Rivera et al, 1998;Stein et al, 2006;Blitz et al, 2017), and muscle contractions are shaped by frequency filtering of neural input (Hooper and Weaver, 2000).…”