Identification of a cellular node for motor control pathways

Levine, Ariel J.; Hinckley, Christopher A.; Hilde, Kathryn L; Driscoll, Shawn P.; Poon, Tiffany; Montgomery, Jessica M.; Pfaff, Samuel L.

doi:10.1038/nn.3675

Cited by 202 publications

(228 citation statements)

References 52 publications

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“…Optical stimulation of ventral glutamatergic neurons at L2 evokes flexor and at L5 extensor bursts (Hägglund et al 2013). Individual motoneuron pools are monosynaptic targets of a premotor column in medial lamina V, believed to encode synergies, with evidence for a rostrocaudal topography (Levine et al 2014). …”

Section: Topography Of Synergiesmentioning

confidence: 99%

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

et al. 2015

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Locomotion is produced by a central pattern generator. Its spinal cord organization is generally considered to be distributed, with more rhythmogenic rostral lumbar segments. While this produces a rostrocaudally traveling wave in undulating species, this is not thought to occur in limbed vertebrates, with the exception of the interneuronal traveling wave demonstrated in fictive cat scratching (Cuellar et al. J Neurosci 29:798-810, 2009). Here, we reexamine this hypothesis in the frog, using the seven muscle synergies A to G previously identified with intraspinal NMDA (Saltiel et al. J Neurophysiol 85:605-619, 2001). We find that locomotion consists of a sequence of synergy activations (A-B-G-A-F-E-G). The same sequence is observed when focal NMDA iontophoresis in the spinal cord elicits a caudal extensionlateral force-flexion cycle (flexion onset without the C synergy). Examining the early NMDA-evoked motor output at 110 sites reveals a rostrocaudal topographic organization of synergy encoding by the lumbar cord. Each synergy is preferentially activated from distinct regions, which may be multiple, and partially overlap between different synergies. Comparing the sequence of synergy activation in locomotion with their spinal cord topography suggests that the locomotor output is achieved by a rostrocaudally traveling wave of activation in the swing-stance cycle. A two-layer circuitry model, based on this topography and a traveling wave reproduces this output and explores its possible modifications under different afferent inputs. Our results and simulations suggest that a rostrocaudally traveling wave of excitation takes advantage of the topography of interneuronal regions encoding synergies, to activate them in the proper sequence for locomotion.

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Section: Topography Of Synergiesmentioning

confidence: 99%

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

et al. 2015

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“…However, there remains heated debate regarding whether these observations reflect a neurophysiological basis or are an epiphenomenon of task constraints and biomechanics (6)(7)(8). This controversy stems from a lack of direct evidence for (or against) the neural implementations of muscle synergies in the CNS (9)(10)(11). Previous studies have suggested that output projections of spinal premotor interneurons (PreM-INs) to motoneuron pools are the neural basis of coordinated muscle activity (10,11).…”

mentioning

confidence: 99%

“…This controversy stems from a lack of direct evidence for (or against) the neural implementations of muscle synergies in the CNS (9)(10)(11). Previous studies have suggested that output projections of spinal premotor interneurons (PreM-INs) to motoneuron pools are the neural basis of coordinated muscle activity (10,11). For example, Hart and Giszter demonstrated in spinalized frogs that PreM-INs have divergent output projections to motoneurons that match the pattern of muscle synergies extracted during spinal motor behaviors (e.g., wiping reflexes) (10).…”

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confidence: 99%

Neural basis for hand muscle synergies in the primate spinal cord

Takei

Confais

Tomatsu

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

143

148

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Grasping is a highly complex movement that requires the coordination of multiple hand joints and muscles. Muscle synergies have been proposed to be the functional building blocks that coordinate such complex motor behaviors, but little is known about how they are implemented in the central nervous system. Here we demonstrate that premotor interneurons (PreM-INs) in the primate cervical spinal cord underlie the spatiotemporal patterns of hand muscle synergies during a voluntary grasping task. Using spike-triggered averaging of hand muscle activity, we found that the muscle fields of PreM-INs were not uniformly distributed across hand muscles but rather distributed as clusters corresponding to muscle synergies. Moreover, although individual PreM-INs have divergent activation patterns, the population activity of PreM-INs reflects the temporal activation of muscle synergies. These findings demonstrate that spinal PreM-INs underlie the muscle coordination required for voluntary hand movements in primates. Given the evolution of neural control of primate hand functions, we suggest that spinal premotor circuits provide the fundamental coordination of multiple joints and muscles upon which more fractionated control is achieved by superimposed, phylogenetically newer, pathways.spinal interneurons | precision grip | muscle synergies | motor control | nonhuman primate

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“…Samuel Pfaff (Salk Institute, La Jolla, USA) described the motor circuitry that coordinates common movement patterns, i.e. the motor synergy encoder (MSE), which is defined by the presence of the transcription factors Tcafp2β and Satb1/2 (Levine et al, 2014). The MSE interneurons coordinate distal and proximal limb MNs.…”

Section: Assembly Of Functional Circuitsmentioning

confidence: 99%

Neural development and regeneration: it's all in your spinal cord

Becker

Corral

2015

Development

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The spinal cord constitutes an excellent model system for studying development and regeneration of a functional nervous system, from specification of its precursors to circuit formation. The latest advances in the field of spinal cord development and its regeneration following damage were discussed at a recent EMBO workshop 'Spinal cord development and regeneration' in Sitges, Spain (October, 2014), highlighting the use of direct visualization of cellular processes, genome-wide molecular techniques and the development of methods for directed stem cell differentiation and regeneration.

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Identification of a cellular node for motor control pathways

Cited by 202 publications

References 52 publications

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

Synergy temporal sequences and topography in the spinal cord: evidence for a traveling wave in frog locomotion

Neural basis for hand muscle synergies in the primate spinal cord

Neural development and regeneration: it's all in your spinal cord

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