Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

Beenhakker, Mark P.; Nusbaum, Michael P.

doi:10.1523/jneurosci.1682-04.2004

Cited by 72 publications

(105 citation statements)

References 52 publications

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“…All previously studied gastric mill rhythms in C. borealis are distinct, despite the fact that they all involve MCN1 activity (Coleman and Nusbaum, 1994;Beenhakker and Nusbaum, 2004;Blitz et al, 2004;Wood et al, 2004). These different rhythms result mainly from differences in the MCN1 activity pattern and/or firing rate, and the level of participation of a second projection neuron, commissural projection neuron 2.…”

Section: Discussionmentioning

confidence: 91%

“…The only difference occurred in the phase of the normalized gastric mill cycle at which the DG neuron burst terminated (n ϭ 11; *p Ͻ 0.01). Nusbaum, 1994;Beenhakker and Nusbaum, 2004;Blitz et al, 2004;Christie et al, 2004;Wood et al, 2004). All of these gastric mill rhythms share several features, including the presence of a two-phase rhythm composed of alternating protractor and retractor phases with a cycle period ranging from 5 to 20 s. There is also rhythmic alternating bursting of the CPG neurons LG and Int1 in all of these rhythms and, in all cases, the retractor neurons VD and DG are coactive with Int1.…”

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 88%

“…In C. borealis, when this rhythm is cycling regularly, it has a cycle period that ranges from ϳ5-20 s both in vivo and in the isolated STNS (Heinzel et al, 1993;Bartos et al, 1999;Beenhakker and Nusbaum, 2004). The gastric mill rhythm is composed of alternating impulse bursts of teeth protractor and retractor motor neurons, plus a single retractor phase Int1 (Fig.…”

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 99%

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Convergent Motor Patterns from Divergent Circuits

Saideman¹,

Blitz²,

Nusbaum³

2007

Journal of Neuroscience

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Neuromodulation changes the cellular and synaptic properties of neurons, thereby enabling individual neuronal circuits to generate multiple activity patterns. However, distinct modulatory inputs could conceivably also configure different motor circuits to generate similar activity patterns. Using the isolated stomatogastric ganglion (STG) of the crab Cancer borealis, we showed previously that pyrokinin (PK) peptides activate the gastric mill (chewing) rhythm without the participation of the projection neuron modulatory commissural neuron 1 (MCN1). MCN1, which does not contain the PK peptide, also activates the gastric mill rhythm and, at these times, is a gastric mill central pattern generator (CPG) neuron. Here, we show that the gastric mill rhythms elicited by PK superfusion and MCN1 stimulation in the isolated STG are comparable, in contrast to the distinct gastric mill rhythms elicited by other input pathways. We also identified several cellular and synaptic mechanisms underlying the PK-and MCN1-elicited gastric mill rhythms that are distinct, including additional differences in their core CPG neurons. For example, the presence of the inhibitory synapse from the pyloric pacemaker neuron anterior burster onto the gastric mill CPG was necessary only for generation of the PK-elicited gastric mill rhythm. Similarly, the dorsal gastric motor neuron regulated only the PK rhythm, apparently because of PK-mediated enhancement of its synaptic actions. Thus, we demonstrate that different modulatory inputs can elicit comparable, as well as distinct activity patterns from the same neuronal ensemble. Moreover, these comparable rhythms can result from distinct CPGs using overlapping, but distinct sets of cellular and synaptic mechanisms.

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Section: Discussionmentioning

confidence: 91%

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 88%

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 99%

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Convergent Motor Patterns from Divergent Circuits

Saideman¹,

Blitz²,

Nusbaum³

2007

Journal of Neuroscience

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“…In rhythmically active networks, proprioceptive and mechanosensory feedback is often coordinated with the activity of central pattern generators (CPGs) and reorganizes their functioning (Beenhakker and Nusbaum, 2004;Büschges, 2005;Cropper et al, 2004;Perrins et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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

Smarandache

Stein

2007

Journal of Experimental Biology

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SUMMARY Sensory input is pervasive among motor networks and continuously adapts motor patterns to changing circumstances. To elucidate common principles of sensorimotor integration, it is beneficial to characterize sensory influences on motor network operation and compare these influences between species. To facilitate such comparison, we have studied the influence of the anterior gastric receptor (AGR) – a proprioceptor that has been characterized in detail in two lobster species – on the pyloric (filtering of food) and gastric mill (chewing of food) motor patterns in the crab Cancer pagurus. AGR has a bipolar cell body in the stomatogastric ganglion; it was activated by tension increase in gastric mill powerstroke muscles. While two spike initiation zones accounted for its spontaneous activity, active membrane properties (sag potentials, spike frequency adaptation) contributed to the AGR response to current injections. When activated, AGR diminished spike activities in two pyloric motor neurons and prolonged the pyloric cycle period. Furthermore, AGR excited gastric mill protractor neurons, inhibited the retractor neuron and evoked phase-independent resetting of the gastric mill rhythm. Repetitive spike trains entrained the rhythm to both longer and shorter cycle periods. All AGR actions seemed to be mediated via at least two premotor projection neurons in the spatially distant commissural ganglia. The response of the gastric mill neurons was independent of AGR firing frequency. Our results suggest that homologous proprioceptors can elicit similar effects on motor patterns while utilizing different mechanisms. This work thus provides an initial framework for future studies to determine underlying common principles.

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“…Numerous examples exist of systems in which the transformation from sensory inputs to motor outputs has been studied (Lee et al, 1988;Schwartz et al, 1988;Fortier et al, 1989;Masino and Knudsen, 1990;Andersen et al, 1993;Britten et al, 1996). The clearest examples are found in invertebrate systems in which the different processing stages between input and output are more directly accessible (Lewis and Kristan, 1998;Levi and Camhi, 2000;Beenhakker and Nusbaum, 2004). Normally, the role of intrinsic dynamics cannot be distinguished from regular sensory coding functions.…”

Section: Introductionmentioning

confidence: 99%

The Role of Sensory Network Dynamics in Generating a Motor Program

Levi¹,

Varona²,

Arshavsky³

et al. 2005

J. Neurosci.

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Sensory input plays a major role in controlling motor responses during most behavioral tasks. The vestibular organs in the marine mollusk Clione, the statocysts, react to the external environment and continuously adjust the tail and wing motor neurons to keep the animal oriented vertically. However, we suggested previously that during hunting behavior, the intrinsic dynamics of the statocyst network produce a spatiotemporal pattern that may control the motor system independently of environmental cues. Once the response is triggered externally, the collective activation of the statocyst neurons produces a complex sequential signal. In the behavioral context of hunting, such network dynamics may be the main determinant of an intricate spatial behavior. Here, we show that (1) during fictive hunting, the population activity of the statocyst receptors is correlated positively with wing and tail motor output suggesting causality, (2) that fictive hunting can be evoked by electrical stimulation of the statocyst network, and (3) that removal of even a few individual statocyst receptors critically changes the fictive hunting motor pattern. These results indicate that the intrinsic dynamics of a sensory network, even without its normal cues, can organize a motor program vital for the survival of the animal.

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Mechanosensory Activation of a Motor Circuit by Coactivation of Two Projection Neurons

Cited by 72 publications

References 52 publications

Convergent Motor Patterns from Divergent Circuits

Convergent Motor Patterns from Divergent Circuits

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

The Role of Sensory Network Dynamics in Generating a Motor Program

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