Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab <i>Cancer borealis</i>

Christie, Andrew E.; Stein, Wolfgang; Quinlan, John E.; Beenhakker, Mark P.; Marder, Eve; Nusbaum, Michael P.

doi:10.1002/cne.11003

Cited by 67 publications

(117 citation statements)

References 88 publications

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“…There were additional qualitative similarities between the MCN1-and PK-elicited gastric mill rhythms, including the presence of IC neuron activity during the LG burst and the absence of bursting in the GM and AM neurons. These features distinguished them from all other previously studied gastric mill rhythms Blitz et al, 2004;Christie et al, 2004;Wood et al, 2004).…”

Section: Discussionmentioning

confidence: 53%

“…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%

“…For example, as shown in Figure 1 B, IC neuron activity was distinct during the MCN1-and ventral cardiac neuron (VCN)-elicited gastric mill rhythms whereas GM neuron bursting occurred only during the VCNelicited rhythm. The MCN1-elicited rhythm is similarly distinct from the rhythms elicited by the gastropyloric receptor (GPR) and inferior ventricular nerve neurons (Blitz et al, 2004;Christie et al, 2004).…”

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 98%

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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: 53%

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 88%

Section: Mcn1 and Pk Peptides Elicit Similar Gastric Mill Rhythmsmentioning

confidence: 98%

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Convergent Motor Patterns from Divergent Circuits

Saideman¹,

Blitz²,

Nusbaum³

2007

Journal of Neuroscience

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“…This VCN gating action was also not a necessary consequence of any recent modulatory action on these projection neurons because, during rhythmic GPR stimulation that drives the gastric mill rhythm, each subsequent GPR stimulation continues to enhance the activity of MCN1 and CPN2 . It remains to be determined whether other pathways that activate a comparable gastric mill rhythm, such as stimulation of the inferior ventricular nerve neurons, also gate this GPR action (Christie et al, 2004).…”

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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“…In C. borealis alone there are at least five projection neurons that elicit different pyloric rhythms when individually stimulated (Norris et al, 1996;Blitz et al, 1999;Christie et al, 2004). With this in mind, sensory regulation of a neuronal circuit could result from its activation of a single projection neuron, a subset of relevant projection neurons, or all relevant projection neurons.…”

mentioning

confidence: 99%

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

Beenhakker¹,

Nusbaum²

2004

J. Neurosci.

102

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Individual neuronal circuits can generate multiple activity patterns because of the influence of different projection neurons. However, in most systems it has been difficult to identify and assess the relative contribution of all upstream neurons responsible for the activation of any single activity pattern by a behaviorally relevant stimulus. To elucidate this issue, we used the stomatogastric nervous system (STNS) of the crab. The STNS includes the gastric mill (chewing) motor circuit in the stomatogastric ganglion (STG) and no more than 20 projection neurons that innervate the STG. We previously identified at least some (four) of the projection neurons that are activated directly by the ventral cardiac neuron (VCN) system, a population of mechanosensory neurons that activates the gastric mill circuit. Here we show that two of these projection neurons, the previously identified modulatory commissural neuron 1 (MCN1) and commissural projection neuron 2 (CPN2), are necessary and likely sufficient for the initiation/maintenance of the VCN-elicited gastric mill rhythm. Selective inactivation of either MCN1 or CPN2 still enabled a VCN-elicited gastric mill rhythm. However, because MCN1 and CPN2 have different actions on gastric mill neurons, these manipulations resulted in rhythms distinct from each other and from that occurring in the intact system. After removal of both MCN1 and CPN2, VCN stimulation failed to activate the gastric mill rhythm. Selective conjoint stimulation of MCN1 and CPN2, approximating their VCN-elicited activity patterns and firing frequencies, elicited a VCN-like gastric mill rhythm. Thus the VCN mechanosensory system elicits the gastric mill rhythm via its activation of a subset of the relevant projection neurons.

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Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab Cancer borealis

Cited by 67 publications

References 88 publications

Convergent Motor Patterns from Divergent Circuits

Convergent Motor Patterns from Divergent Circuits

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

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

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