Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse

Falgairolle, Mélanie; Puhl, Joshua G.; Pujala, Avinash; Liu, Wenfang; O’Donovan, Michael J.

doi:10.7554/elife.26622

Cited by 48 publications

(57 citation statements)

References 79 publications

(112 reference statements)

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“…In newborn rodent, antidromic stimulation of motoneuron via ventral roots can induce rhythmic locomotor-like activity (340) and entrain the spontaneous rhythmic activity induced (51). In neonate mouse, optogenetic manipulation of the activity of motoneurons during ongoing drug-induced locomotor activity also altered the frequency, phase, and stability of the rhythm (159). Similar to zebrafish, when motoneurons were inhibited or activated optogenetically, there was a strong influence on the frequency of the locomotor rhythm.…”

Section: Motoneurons Are Bona Fide Members Of the Cpg: Evidence From mentioning

confidence: 99%

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Grillner

Manira

2020

Physiological Reviews

336

395

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The vertebrate control of locomotion involves all levels of the nervous system from cortex to the spinal cord. Here, we aim to cover all main aspects of this complex behavior, from the operation of the microcircuits in the spinal cord to the systems and behavioral levels and extend from mammalian locomotion to the basic undulatory movements of lamprey and fish. The cellular basis of propulsion represents the core of the control system, and it involves the spinal central pattern generator networks (CPGs) controlling the timing of different muscles, the sensory compensation for perturbations, and the brain stem command systems controlling the level of activity of the CPGs and the speed of locomotion. The forebrain and in particular the basal ganglia are involved in determining which motor programs should be recruited at a given point of time and can both initiate and stop locomotor activity. The propulsive control system needs to be integrated with the postural control system to maintain body orientation. Moreover, the locomotor movements need to be steered so that the subject approaches the goal of the locomotor episode, or avoids colliding with elements in the environment or simply escapes at high speed. These different aspects will all be covered in the review.

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Section: Motoneurons Are Bona Fide Members Of the Cpg: Evidence From mentioning

confidence: 99%

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Grillner

Manira

2020

Physiological Reviews

336

395

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“…In neonatal animals, VR stimulation can induce fictive locomotion (Mentis et al, 2005) and 153 entrain the spontaneous rhythmic bursting induced by block of inhibition (Bonnot et al, 2009). 154 Furthermore, optogenetic activation or silencing of motor pools alters the frequency and phase 155 of chemically induced fictive locomotion (Falgairolle et al, 2017). These effects cannot be 156 7 explained solely by recurrent excitation and may provide evidence for Mn collaterals con-157 tacting unidentified interneurones (Machacek and Hochman, 2006).…”

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confidence: 99%

Recurrent excitation between motoneurones propagates across segments and is purely glutamatergic

Bhumbra

Beato

2017

Preprint

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Spinal motoneurones constitute the final output for the execution of motor tasks. In addition to innervating muscles, motoneurones project excitatory collateral connections to Renshaw cells and other motoneurones, but the latter have received little attention. We show that motoneurones receive strong synaptic input from other motoneurones throughout development and into maturity with fast type motoneurones systematically receiving greater recurrent excitation than slow type motoneurones. Optical recordings show that activation of motoneurones in one spinal segment can propagate to adjacent segments even in the presence of intact recurrent inhibition. Quite remarkably, while it is known that transmission at the neuromuscular junction is purely cholinergic and Renshaw cells are excited through both acetylcholine and glutamate receptors, here we show that neurotransmission between motoneurones is purely glutamatergic indicating that synaptic transmission systems are differentiated at different post-synaptic targets of motoneurones.

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“…Indeed, it recently has been reported that a motoneuronal depolarization increases the locomotor rhythm (Falgairolle, Puhl, Pujala, Liu, & O'Donovan, 2017). Overall, histamine reduces rhythm, despite augmenting excitability of motoneurons, thus suggesting that premotor interneurons are also modulated by histamine.…”

Section: Discussionmentioning

confidence: 97%

“…This result is in accordance with the decreased polysynaptic reflex and lower frequency discharge of tonic activity from VRs, but somehow in contradiction with the increased excitability of spinal motoneurons. Indeed, it recently has been reported that a motoneuronal depolarization increases the locomotor rhythm (Falgairolle, Puhl, Pujala, Liu, & O'Donovan, ). Overall, histamine reduces rhythm, despite augmenting excitability of motoneurons, thus suggesting that premotor interneurons are also modulated by histamine.…”

Section: Discussionmentioning

confidence: 99%

Histamine modulates spinal motoneurons and locomotor circuits

Coslovich

Brumley

D’Angelo

et al. 2017

J of Neuroscience Research

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Spinal motoneurons and locomotor networks are regulated by monoamines, among which, the contribution of histamine has yet to be fully addressed. The present study investigates histaminergic regulation of spinal activity, combining intra- and extracellular electrophysiological recordings from neonatal rat spinal cord in vitro preparations. Histamine dose-dependently and reversibly generated motoneuron depolarization and action potential firing. Histamine (20 µM) halved the area of dorsal root reflexes and always depolarized motoneurons. The majority of cells showed a transitory repolarization, while 37% showed a sustained depolarization maintained with intense firing. Extracellularly, histamine depolarized ventral roots (VRs), regardless of blockage of ionotropic glutamate receptors. Initial, transient glutamate-mediated bursting was synchronous among VRs, with some bouts of locomotor activity in a subgroup of preparations. After washout, the amplitude of spontaneous tonic discharges increased. No desensitization or tachyphylaxis appeared after long perfusion or serial applications of histamine. On the other hand, histamine induced single motoneuron and VR depolarization, even in the presence of tetrodotoxin (TTX). During chemically induced fictive locomotion (FL), histamine depolarized VRs. Histamine dose-dependently increased rhythm periodicity and reduced cycle amplitude until near suppression. This study demonstrates that histamine induces direct motoneuron membrane depolarization and modulation of locomotor output, indicating new potential targets for locomotor neurorehabilitation.

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Motoneurons regulate the central pattern generator during drug-induced locomotor-like activity in the neonatal mouse

Cited by 48 publications

References 79 publications

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion

Recurrent excitation between motoneurones propagates across segments and is purely glutamatergic

Histamine modulates spinal motoneurons and locomotor circuits

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