A newly identified extrinsic input triggers a distinct gastric mill rhythmviaactivation of modulatory projection neurons

Abstract

SUMMARYNeuronal network flexibility enables animals to respond appropriately to changes in their internal and external states. We are using the isolated crab stomatogastric nervous system to determine how extrinsic inputs contribute to network flexibility. The stomatogastric system includes the well-characterized gastric mill (chewing) and pyloric (filtering of chewed food) motor circuits in the stomatogastric ganglion. Projection neurons with somata in the commissural ganglia (CoGs) regulate these rhythms. Previous work characterized a unique gastric mill rhythm that occurred spontaneously in some preparations, but whose origin remained undetermined. This rhythm includes a distinct protractor phase activity pattern, during which a key gastric mill circuit neuron (LG neuron) and the projection neurons MCN1 and CPN2 fire in a pyloric rhythm-timed activity pattern instead of the tonic firing pattern exhibited by these neurons during previously studied gastric mill rhythms. Here we identify a new extrinsic input, the post-oesophageal commissure (POC) neurons, relatively brief stimulation (30·s) of which triggers a long-lasting (tens of minutes) activation of this novel gastric mill rhythm at least in part via its lasting activation of MCN1 and CPN2. Immunocytochemical and electrophysiological data suggest that the POC neurons excite MCN1 and CPN2 by release of the neuropeptide Cancer borealis tachykinin-related peptide Ia (CabTRP Ia). These data further suggest that the CoG arborization of the POC neurons comprises the previously identified anterior commissural organ (ACO), a CabTRP Ia-containing neurohemal organ. This endocrine organ thus appears to also have paracrine actions, including activation of a novel and lasting gastric mill rhythm.

Consequences of acute and long-term removal of neuromodulatory input on the episodic gastric rhythm of the crabCancer borealis

“…containing the modulatory somata (Blitz and Nusbaum 2012;Nusbaum et al 1992). Previous work has demonstrated a rich diversity of roles for these projection neurons in driving and shaping gastric behavior, as well as influencing interactions between the pyloric and gastric rhythms White and Nusbaum 2011;Wood et al 2004).…”

“…The episodic gastric network may provide a better model for vertebrate spinal injury, where the affected CPGs for locomotion are episodically active. Although the gastric rhythm depends heavily on interactions with descending inputs (Bartos et al 1999;Blitz et al 1999;Blitz and Nusbaum 2012;Dickinson et al 1988;Nadim et al 1998;Nusbaum and Beenhakker 2002), surprisingly, rhythmic activity in some gastric neurons persists in long-term recordings. Consequently, in this report we quantitatively describe a number of features of the rhythmic activity in gastric neurons in long-term (many days) recordings of STG preparations.…”

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).…”

Sources and range of long-term variability of rhythmic motor patternsin vivo.

“…During this type of rhythm, LG bursts display continuous spiking. In contrast, when the peptidergic postoesophageal commissure neurons (POCs) are activated, the LG burst firing is interrupted periodically and consists of shorter burstlets (Blitz et al, 2008). The type 1 gastric mill rhythm showed both types of bursts, and seamlessly switched back and forth between them.…”