Sensory-induced modification of two motor patterns in the crab,<i>Cancer pagurus</i>

Smarandache, Carmen; Stein, Wolfgang

doi:10.1242/jeb.006874

Cited by 35 publications

(74 citation statements)

References 35 publications

(66 reference statements)

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“…The tonically active unit in the dgn corresponds to the activity of the anterior gastric receptor (AGR) neuron. AGR is a muscle tendon proprioceptor neuron that is spontaneously active in the isolated STNS (Combes et al, 1995;Smarandache and Stein, 2007). Most hyperpolarized Vm: MCN1, Ϫ44 mV.…”

Section: Discussionmentioning

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: Discussionmentioning

confidence: 99%

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

Beenhakker¹,

Kirby²,

Nusbaum³

2007

J. Neurosci.

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“…The large, tonically active unit in the dgn corresponds to the activity of the anterior gastric receptor (AGR) neuron. AGR is a muscle tendon proprioceptor neuron that is spontaneously active in the isolated STNS (Combes et al, 1995;Smarandache and Stein, 2007). (Middle) 2·min after tonic poc stimulation (15·Hz, 30·s), the gastric mill rhythm was triggered, as is evident from the rhythmic bursting in the protractor LG neuron that alternated with the retractor phase activity of the DG, VD and IC neurons.…”

Section: Poc Stimulation Triggers a Long-lasting Gastric Mill Rhythmmentioning

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

144

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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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“…pagurus physiological saline had the following composition (mmol l -1 ): NaCl, 440; MgCl 2 , 26; CaCl 2 , 13; KCl, 11; Trizma base, 10; maleic acid, 5, pH 7.4-7.6. In some experiments, high divalent saline (5ϫ Ca 2+ /5ϫ Mg 2+ ) was applied exclusively to the CoG to block polysynaptic connections (Blitz and Nusbaum, 1999;Smarandache and Stein, 2007).…”

Section: Solutionsmentioning

confidence: 99%

“…Extracellular recordings in vitro were obtained as described previously (Smarandache and Stein, 2007); that is, by electrically isolating individual sections of STNS nerves from the bath by building a petroleum jelly-based cylindrical compartment around a section of the nerve. The action potentials propagating through the nerve were recorded by placing one of two stainless steel electrode wires within this compartment.…”

Section: Electrophysiology and Preparationsmentioning

confidence: 99%

“…Our results thus indicate that projection neurons located in the CoG are involved in the processing of exteroceptive sensory information. These neurons are well known to process proprioceptive and mechanosensory information Simmers and Moulins, 1988a;Simmers and Moulins, 1988b;Smarandache and Stein, 2007) from sense organs within the stomatogastric system. It is thus conceivable that they represent a point of multisensory convergence, processing information from proprioceptors and exteroceptors.…”

Section: Effect On the Motor Patternsmentioning

confidence: 99%

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Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system

Hedrich

Stein

2008

Journal of Experimental Biology

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SUMMARYThe regulation of motor patterns by higher-order neuronal centers ensures appropriate motor function and behavior, but only a few studies have characterized this regulation at the cellular level. Here, we address motor pattern regulation in the stomatogastric nervous system (STNS) of the crab Cancer pagurus. This easily accessible model system is an extension of the central nervous system and contains the motor circuits that generate the rhythmic motor patterns for ingestion (esophageal rhythm) and processing of food (gastric mill and pyloric rhythms).We have documented the actions of two identified neurons located in the brain on the STNS motor circuits. We show that these neurons provide exteroceptive chemosensory information to the motor circuits and we outline their axonal projection patterns, their firing activity and their effects on three motor patterns. Backfill stainings and activity measurements in vivo and in vitro show that two neurons located in cluster 17 of the brain project via the inferior ventricular (IV) nerve to the STNS. These IV neurons started to burst rhythmically when chemosensory stimuli were applied to the first antennae. When rhythmically activated in vitro, gastric mill rhythms were elicited or, if already active, entrained by the IV neuron activity. In addition, IV neuron stimulation excited the esophageal motor neuron and inhibited several pyloric neurons such that the timing of the IV neuron activity was imposed on all motor rhythms. The IV neurons were thus capable of synchronizing the activities of different motor circuits, which demonstrates the regulation of motor patterns by higher-order neuronal centers.

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Sensory-induced modification of two motor patterns in the crab,Cancer pagurus

Cited by 35 publications

References 35 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

Characterization of a descending pathway: activation and effects on motor patterns in the brachyuran crustacean stomatogastric nervous system

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