Parallel Regulation of a Modulator-Activated Current via Distinct Dynamics Underlies Comodulation of Motor Circuit Output

DeLong, Nicholas D.; Kirby, Matthew S.; Blitz, Dawn M.; Nusbaum, Michael P.

doi:10.1523/jneurosci.3079-09.2009

Cited by 43 publications

(134 citation statements)

References 53 publications

(146 reference statements)

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“…Invertebrates, with their simple and accessible nervous systems, have long been useful for elucidating synaptic connectivity within central pattern generating networks (Nusbaum and Beenhakker 2002) and how motor patterns are modulated and selected (DeLong et al 2009). Here we use the leech heartbeat CPG to assess how motoneuron intrinsic properties and electrical coupling contribute to rhythmic motor output.…”

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confidence: 99%

Contribution of motoneuron intrinsic properties to fictive motor pattern generation

Wright

Calabrese

2011

Journal of Neurophysiology

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Wright TM Jr, Calabrese RL. Contribution of motoneuron intrinsic properties to fictive motor pattern generation. J Neurophysiol 106: 538-553, 2011. First published May 11, 2011 doi:10.1152/jn.00101.2011.-Previously, we reported a canonical ensemble model of the heart motoneurons that underlie heartbeat in the medicinal leech. The model motoneurons contained a minimal set of electrical intrinsic properties and received a synaptic input pattern based on measurements performed in the living system. Although the model captured the synchronous and peristaltic motor patterns observed in the living system, it did not match quantitatively the motor output observed. Because the model motoneurons had minimal intrinsic electrical properties, the mismatch between model and living system suggests a role for additional intrinsic properties in generating the motor pattern. We used the dynamic clamp to test this hypothesis. We introduced the same segmental input pattern used in the model to motoneurons isolated pharmacologically from their endogenous input in the living system. We show that, although the segmental input pattern determines the segmental phasing differences observed in motoneurons, the intrinsic properties of the motoneurons play an important role in determining their phasing, particularly when receiving the synchronous input pattern. We then used trapezoidal input waveforms to show that the intrinsic properties present in the living system promote phase advances compared with our model motoneurons. Electrical coupling between heart motoneurons also plays a role in shaping motoneuron output by synchronizing the activity of the motoneurons within a segment. These experiments provide a direct assessment of how motoneuron intrinsic properties interact with their premotor pattern of synaptic drive to produce rhythmic output.

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confidence: 99%

Contribution of motoneuron intrinsic properties to fictive motor pattern generation

Wright

Calabrese

2011

Journal of Neurophysiology

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“…Like CCAP, applied DA likely provides tonic excitation that enhances the phasic MCN1 excitation of LG (Delong et al 2009b;Kirby and Nusbaum 2007). Similar to CCAP actions, DA likely has no influence on Int1 during MCN1 activation (Kirby and Nusbaum 2007), and this unbalanced LG excitation allows it to more effectively escape from Int1 inhibition.…”

Section: Discussionmentioning

confidence: 96%

“…MCN1's peptide cotransmitters are known to activate a nonselective cationic current in pyloric and gastric mill neurons (Delong et al 2009b;Golowasch and Marder 1992;Swensen and Marder 2000). This current appears distinct from those modulated by DA.…”

Section: Discussionmentioning

confidence: 98%

“…Our preliminary studies show that MCN1 does not contain DA (Wood, unpublished data), suggesting that MCN1 actions and DA actions on currents are distinct. In the CCAP modulated MCN1 elicited rhythm, enhanced protraction with decreased retraction occurs because CCAP tonically increases the peptide activated current in the LG neuron (Delong et al 2009b). Whether the actions of MCN1 cotransmitters are entirely parallel or overlap with DA actions remains to be determined.…”

Section: Discussionmentioning

confidence: 98%

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Hormonal Modulation of Two Coordinated Rhythmic Motor Patterns

Wood

Varrecchia

Papernov

et al. 2010

Journal of Neurophysiology

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Wood DE, Varrecchia M, Papernov M, Cook D, Crawford DC. Hormonal modulation of two coordinated rhythmic motor patterns. J Neurophysiol 104: 654 -664, 2010. First published June 2, 2010 doi:10.1152/jn.00846.2009. Neuromodulation is well known to provide plasticity in pattern generating circuits, but few details are available concerning modulation of motor pattern coordination. We are using the crustacean stomatogastric nervous system to examine how co-expressed rhythms are modulated to regulate frequency and maintain coordination. The system produces two related motor patterns, the gastric mill rhythm that regulates protraction and retraction of the teeth and the pyloric rhythm that filters food. These rhythms have different frequencies and are controlled by distinct mechanisms, but each circuit influences the rhythm frequency of the other via identified synaptic pathways. A projection neuron, MCN1, activates distinct versions of the rhythms, and we show that hormonal dopamine concentrations modulate the MCN1 elicited rhythm frequencies. Gastric mill circuit interactions with the pyloric circuit lead to changes in pyloric rhythm frequency that depend on gastric mill rhythm phase. Dopamine increases pyloric frequency during the gastric mill rhythm retraction phase. Higher gastric mill rhythm frequencies are associated with higher pyloric rhythm frequencies during retraction. However, dopamine slows the gastric mill rhythm frequency despite the increase in pyloric frequency. Dopamine reduces pyloric circuit influences on the gastric mill rhythm and upregulates activity in a gastric mill neuron, DG. Strengthened DG activity slows the gastric mill rhythm frequency and effectively reduces pyloric circuit influences, thus changing the frequency relationship between the rhythms. Overall dopamine shifts dependence of frequency regulation from intercircuit interactions to increased reliance on intracircuit mechanisms.

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“…Bath applying CabTRP Ia to the isolated STG elicits a m odulator-activated, i nward, voltage-dependent ionic current ( I MI ) in the LG neuron (DeLong et al, 2009b). Bath application of the peptide hormone, crustacean cardioactive peptide (CCAP), to the isolated STG also activates I MI in the LG neuron (DeLong et al, 2009b).…”

Section: Introductionmentioning

confidence: 99%

Convergent neuromodulation onto a network neuron can have divergent effects at the network level

2016

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Different neuromodulators often target the same ion channel. When such modulators act on different neuron types, this convergent action can enable a rhythmic network to produce distinct outputs. Less clear are the functional consequences when two neuromodulators influence the same ion channel in the same neuron. We examine the consequences of this seeming redundancy using a mathematical model of the crab gastric mill (chewing) network. This network is activated in vitro by the projection neuron MCN1, which elicits a half-center bursting oscillation between the reciprocally-inhibitory neurons LG and Int1. We focus on two neuropeptides which modulate this network, including a MCN1 neurotransmitter and the hormone crustacean cardioactive peptide (CCAP). Both activate the same voltage-gated current (IMI) in the LG neuron. However, IMI-MCN1, resulting from MCN1 released neuropeptide, has phasic dynamics in its maximal conductance due to LG presynaptic inhibition of MCN1, while IMI-CCAP retains the same maximal conductance in both phases of the gastric mill rhythm. Separation of time scales allows us to produce a 2D model from which phase plane analysis shows that, as in the biological system, IMI-MCN1 and IMI-CCAP primarily influence the durations of opposing phases of this rhythm. Furthermore, IMI-MCN1 influences the rhythmic output in a manner similar to the Int1-to-LG synapse, whereas IMI-CCAP has an influence similar to the LG-to-Int1 synapse. These results show that distinct neuromodulators which target the same voltage-gated ion channel in the same network neuron can nevertheless produce distinct effects at the network level, providing divergent neuromodulator actions on network activity.

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Parallel Regulation of a Modulator-Activated Current via Distinct Dynamics Underlies Comodulation of Motor Circuit Output

Cited by 43 publications

References 53 publications

Contribution of motoneuron intrinsic properties to fictive motor pattern generation

Contribution of motoneuron intrinsic properties to fictive motor pattern generation

Hormonal Modulation of Two Coordinated Rhythmic Motor Patterns

Convergent neuromodulation onto a network neuron can have divergent effects at the network level

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