Contribution of motoneuron intrinsic properties to fictive motor pattern generation

Wright, Terrence Michael; Calabrese, Ronald L.

doi:10.1152/jn.00101.2011

Cited by 23 publications

(22 citation statements)

References 41 publications

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“…In the synchronous mode, although the model motor neurons can approximate the target phase (Tables 1, 2), the range of phases where this occurs appears to be restricted to preparations in which we observed HE(8) phases delayed substantially from the average of the physiological data set; therefore, the model motor neurons will need to be modified in such a way as to promote a phase advance by initiating their burst firing as premotor inhibitory input wanes (Fig. 1), as suggested previously (Wright and Calabrese, 2011). …”

Section: Resultsmentioning

confidence: 51%

Patterns of Presynaptic Activity and Synaptic Strength Interact to Produce Motor Output

Wright¹,

Calabrese²

2011

J. Neurosci.

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Motor neuron activity is coordinated by premotor networks into a functional motor pattern by complex patterns of synaptic drive. These patterns combine both the temporal pattern of spikes of the premotor network and the profiles of synaptic strengths (i.e., conductances). Given the complexity of premotor networks in vertebrates, it has been difficult to ascertain the relative contributions of temporal patterns and synaptic strength profiles to the motor patterns observed in these animals. Here, we use the leech (Hirudo sp.) heartbeat central pattern generator (CPG), in which we can measure both the temporal pattern and the synaptic strength profiles of the entire premotor network and the motor outflow in individual animals. In this system, a series of motor neurons all receive input from the same premotor interneurons of the CPG but must be coordinated differentially to produce a functional pattern. These properties allow a theoretical and experimental dissection of the rules that govern how temporal patterns and synaptic strength profiles are combined in motor neurons so that functional motor patterns emerge, including an analysis of the impact of animal-to-animal variation in input to such variation in output. In the leech, segmental heart motor neurons are coordinated alternately in a synchronous and peristaltic pattern. We show that synchronous motor patterns result from a nearly synchronous premotor temporal pattern produced by the leech heartbeat CPG. For peristaltic motor patterns, the staggered premotor temporal pattern determines the phase range over which segmental motor neurons can fire while synaptic strength profiles define the intersegmental motor phase progression realized.

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Section: Resultsmentioning

confidence: 51%

Patterns of Presynaptic Activity and Synaptic Strength Interact to Produce Motor Output

Wright¹,

Calabrese²

2011

J. Neurosci.

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“…In this context, their membrane properties play a critical role in processing brainstem inputs, determining the respiratory motoneurons output and resultant respiratory motor activity (Iscoe, ; de Almeida et al . ; Wright & Calabrese, ; Road et al . ).…”

Section: Introductionmentioning

confidence: 99%

“…Therefore, motoneurons should integrate, amplify and propagate all dendritic electrical oscillations to the cell soma to ensure an appropriate action potential generation. In this context, their membrane properties play a critical role in processing brainstem inputs, determining the respiratory motoneurons output and resultant respiratory motor activity (Iscoe, 1998;de Almeida et al 2010;Wright & Calabrese, 2011;Road et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Hyperexcitability and plasticity induced by sustained hypoxia on rectus abdominis motoneurons

Silva

Moraes

Bonagamba

et al. 2019

The Journal of Physiology

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Key points Acute hypoxia induces active expiration in rectus abdominis (RA) muscles in conscious freely moving rats, although its overall contribution is smaller than in internal oblique (IO) muscles. Tonically active and silent RA motoneurons were identified in in vitro preparations of rat spinal cords. Sustained hypoxia (SH) increased the synaptic strength and induced morphological changes in tonically active RA motoneurons. Expiratory RA motoneurons were recorded in the in situ preparation and SH enhanced both the excitability and the synaptic transmission in those firing during the stage 2 expiration. The present study contributes to a better understanding of the mechanisms involved in SH recruitment of RA motoneurons to induce active expiration in rats. Abstract Rectus abdominis (RA) motoneurons translate the complex respiratory brainstem inputs into effective muscle contractions. Despite their fundamental role in respiration, their functional and morphological properties are not fully understood. In the present study, we investigated for the first time the contribution of RA muscle to active expiration and characterized RA motoneurons regarding their electrical, molecular and morphological profiles in control rats and in rats submitted to sustained hypoxia (SH), which induces chronic recruitment of abdominal muscles. Electromyographic experiments in conscious freely moving control rats and SH rats showed that RA contributes to active expiration induced by acute hypoxia, although its contribution is smaller than in internal oblique muscles. in vitro whole‐cell patch clamp recordings from RA motoneurons revealed two populations of cells: tonically active and silent. SH induced hyperexcitability in the tonically active cells by changing their action potential properties, and EPSCs. Three‐dimensional morphological reconstructions of these cells showed that SH increased the dendritic complexity, stimulated the appearance of dendrite spines, and increased the somatic area and volume. Physiologically identified RA motoneurons, firing in two distinct phases of expiration, were recorded in the brainstem–spinal cord in situ preparation of rats. SH increased the firing frequency and EPSCs of neurons firing during stage 2 expiration. Taken together, our results show that RA motoneurons reconfigure their biophysical properties, morphology and synaptic strength to produce an appropriate expiratory drive in response to SH in rats.

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“…In many systems, motor neurons (MNs) are not part of the classically-defined CPG network (Marder & Bucher, 2001). However, intrinsic MN properties, such as specific ionic currents, may play a crucial role in producing proper motor output (del Negro, Hsiao & Chandler, 1999; Gorassini et al, 1999; Hounsgaard et al, 1984; Wright & Calabrese, 2011) (for reviews see Harris-Warrick (2002), Heckman et al (2009), Kiehn et al (2000) and Marder & Goaillard (2006)). To what extent MN currents shape the motor pattern, and exactly how aspects of the pattern are altered by expression of specific ion channel genes, are open questions.…”

Section: Introductionmentioning

confidence: 99%

Effects of manipulating slowpoke calcium-dependent potassium channel expression on rhythmic locomotor activity inDrosophilalarvae

McKiernan

2013

PeerJ

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Rhythmic motor behaviors are generated by networks of neurons. The sequence and timing of muscle contractions depends on both synaptic connections between neurons and the neurons’ intrinsic properties. In particular, motor neuron ion currents may contribute significantly to motor output. Large conductance Ca2+-dependent K+ (BK) currents play a role in action potential repolarization, interspike interval, repetitive and burst firing, burst termination and interburst interval in neurons. Mutations in slowpoke (slo) genes encoding BK channels result in motor disturbances. This study examined the effects of manipulating slo channel expression on rhythmic motor activity using Drosophila larva as a model system. Dual intracellular recordings from adjacent body wall muscles were made during spontaneous crawling-related activity in larvae expressing a slo mutation or a slo RNA interference construct. The incidence and duration of rhythmic activity in slo mutants were similar to wild-type control animals, while the timing of the motor pattern was altered. slo mutants showed decreased burst durations, cycle durations, and quiescence intervals, and increased duty cycles, relative to wild-type. Expressing slo RNAi in identified motor neurons phenocopied many of the effects observed in the mutant, including decreases in quiescence interval and cycle duration. Overall, these results show that altering slo expression in the whole larva, and specifically in motor neurons, changes the frequency of crawling activity. These results suggest an important role for motor neuron intrinsic properties in shaping the timing of motor output.

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Contribution of motoneuron intrinsic properties to fictive motor pattern generation

Cited by 23 publications

References 41 publications

Patterns of Presynaptic Activity and Synaptic Strength Interact to Produce Motor Output

Patterns of Presynaptic Activity and Synaptic Strength Interact to Produce Motor Output

Hyperexcitability and plasticity induced by sustained hypoxia on rectus abdominis motoneurons

Effects of manipulating slowpoke calcium-dependent potassium channel expression on rhythmic locomotor activity inDrosophilalarvae

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