Divergent co‐transmitter actions underlie motor pattern activation by a modulatory projection neuron

Stein, Wolfgang; DeLong, Nicholas D.; Wood, Debra E.; Nusbaum, Michael P.

doi:10.1111/j.1460-9568.2007.05744.x

Cited by 70 publications

(115 citation statements)

References 52 publications

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“…In this species, there are ϳ20 such projection neurons, each of which is likely present as a single neuron in each CoG (Coleman et al, 1992). Four of these projection neurons, including MCN1, MCN5, MCN7, and CPN2, are identified, and at least some of their actions on the STG are characterized Norris et al, 1994Norris et al, , 1996Coleman et al, 1995;Blitz et al, 1999;Stein et al, 2007). All four of these CoG neurons are excited, albeit to different extents, by stimulation of either the VCNs or GPR Blitz et al, 2004).…”

Section: Mcn1 and Cpn2 Are Necessary And Sufficient To Drive The Vcn-mentioning

confidence: 99%

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

Beenhakker¹,

Kirby²,

Nusbaum³

2007

J. Neurosci.

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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.

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Section: Mcn1 and Cpn2 Are Necessary And Sufficient To Drive The Vcn-mentioning

confidence: 99%

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

Beenhakker¹,

Kirby²,

Nusbaum³

2007

J. Neurosci.

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“…In C. borealis there are eight different types of gastric mill neurons, seven of which are motor neurons (Weimann et al, 1991;Saideman et al, 2007b;Stein et al, 2007). Four of these gastric mill neurons are protractor motor neurons, including the LG, GM, medial gastric (MG) and inferior cardiac (IC) neurons, although the IC and MG neurons can also exhibit retractor phase activity during some versions of the gastric mill rhythm Blitz et al, 2004;Wood et al, 2004;Saideman et al, 2007b).…”

Section: The Gastric Mill Rhythm Is a Two-phase Motor Pattern Driven mentioning

confidence: 99%

“…To this end, we applied the endopeptidase inhibitor phosphoramidon (10 -5 ·mol·l -1 ), which effectively prolongs the actions of both focally applied and neuronally released CabTRP Ia (Wood et al, 2000;Stein et al, 2007). Because the poc stimulus protocol used to trigger the gastric mill rhythm had such a longlasting effect, we used briefer poc stimulations (15·Hz, 15·s) to achieve relatively brief control responses.…”

Section: The Poc Neurons Appear To Use the Peptide Transmitter Cabtrp Iamentioning

confidence: 99%

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

Blitz

White

Saideman

et al. 2008

Journal of Experimental Biology

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142

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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.

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“…Specifically, when the descending projection neuron, modulatory commissural neuron 1 (MCN1), is selectively activated, the pyloric rhythm speeds up (Stein et al, 2007). Pyloric cycle frequency is additionally modulated with the phasing of the MCN1-activated gastric mill rhythm: pyloric cycle frequency diminishes during LG neuron bursts and speeds up during the LG inter-burst (Coleman et al, 1995).…”

Section: Resultsmentioning

confidence: 99%

“…In vitro, when the gastric mill rhythm is activated via extrinsic inputs (such as descending projection neurons), the cycle frequency of the pyloric rhythm increases (Coleman et al, 1995;Stein et al, 2007;Stein, 2009). Specifically, when the descending projection neuron, modulatory commissural neuron 1 (MCN1), is selectively activated, the pyloric rhythm speeds up (Stein et al, 2007).…”

Section: Resultsmentioning

confidence: 99%

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

Yarger

Stein

2015

Journal of Experimental Biology

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The mechanisms of rhythmic motor pattern generation have been studied in detail in vitro, but the long-term stability and sources of variability in vivo are often not well described. The crab stomatogastric ganglion contains the well-characterized gastric mill (chewing) and pyloric (filtering of food) central pattern generators. In vitro, the pyloric rhythm is stereotyped with little variation, but intercircuit interactions and neuromodulation can alter both rhythm cycle frequency and structure. The range of variation of activity in vivo is, with few exceptions, unknown. Curiously, although the patterngenerating circuits in vivo are constantly exposed to hormonal and neural modulation, the majority of published data show only the unperturbed canonical motor patterns typically observed in vitro. Using long-term extracellular recordings (N=27 animals), we identified the range and sources of variability of the pyloric and gastric mill rhythms recorded continuously over 4 days in freely behaving Jonah crabs (Cancer borealis). Although there was no evidence of innate daily rhythmicity, a 12 h light-driven cycle did manifest. The frequency of both rhythms increased modestly, albeit consistently, during the 3 h before and 3 h after the lights changed. This cycle was occluded by sensory stimulation (feeding), which significantly influenced both pyloric cycle frequency and structure. This was the only instance where the structure of the rhythm changed. In unfed animals the structure remained stable, even when the frequency varied substantially. So, although central pattern generating circuits are capable of producing many patterns, in vivo outputs typically remain stable in the absence of sensory stimulation.

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Divergent co‐transmitter actions underlie motor pattern activation by a modulatory projection neuron

Cited by 70 publications

References 52 publications

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

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

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

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