Spinal Interneurons Facilitate Coactivation of Hand Muscles during a Precision Grip Task in Monkeys

Takei, Toshinobu; Seki, Kazuhiko

doi:10.1523/jneurosci.4297-10.2010

Cited by 105 publications

(97 citation statements)

References 65 publications

(82 reference statements)

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“…Two macaque monkeys were trained to perform a precision grip task, in which they were required to grip and release two springloaded levers with their index finger and thumb to target positions (12,16). During the task, we recorded single-unit activity from cervical spinal neurons and electromyographic (EMG) activity from 12 hand muscles (Fig.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Neural basis for hand muscle synergies in the primate spinal cord

Takei

Confais

Tomatsu

et al. 2017

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

138

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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Section: Resultsmentioning

confidence: 99%

“…We previously showed that PreM-INs in monkey cervical cords have divergent postspike effects on a group of hand muscles during a precision grip task, termed the neuron's "muscle field" (12). This finding suggests that PreM-INs contribute to the synergistic control of primate hand movements (9,(13)(14)(15), but this question has not been examined directly.…”

mentioning

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.

138

148

View full text Add to dashboard Cite

show abstract

“…In primates and rodents there is evidence for the role of spinal interneurons in regulating hand movements. [30][31][32] Our injury paradigm results in significant loss of GM in the C6 region, which contains motor neurons and interneurons that make up spinal circuits responsible for forelimb and hand movement. We propose that permanent neuronal loss in forelimb spinal circuits results in functional deficits that cannot be overcome by natural recovery.…”

Section: Discussionmentioning

confidence: 99%

Bilateral Contusion-Compression Model of Incomplete Traumatic Cervical Spinal Cord Injury

Forgione

Karadimas

Foltz

et al. 2014

Journal of Neurotrauma

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Despite the increasing incidence and prevalence of cervical spinal cord injury (cSCI), we lack clinically relevant animal models that can be used to study the pathomechanisms of this injury and test new therapies. Here, we characterize a moderate cervical contusion-compression model in rats that is similar to incomplete traumatic cSCI in humans. We characterized the effects of 18-g clip-compression injury at cervical level C6 over an 8-week recovery period. Using Luxol fast blue/hematoxylin-eosin staining in combination with quantitative stereology, we determined that 18-g injury results in loss of gray matter (GM), white matter (WM), as well as in cavity formation. Magnetization transfer and T2-weighted magnetic resonance imaging were used to analyze lesion dynamics in vivo. This analysis demonstrated that both techniques are able to differentiate between the injury epicenter, subpial rim, and WM distal to the injury. Neurobehavioral assessment of locomotor function using Basso, Beattie, and Bresnahan (BBB) scoring and CatWalk revealed limited recovery from clip-compression injury at C6. Testing of forelimb function using grip strength demonstrated significant forelimb dysfunction, similar to the loss of upper-limb motor function observed in human cSCI. Sensory-evoked potentials recorded from the forelimb and Hoffman reflex recorded from the hindlimb confirmed the fore-and hindlimb deficits observed in our neurobehavioral analysis. Here, we have characterized a clip-compression model of incomplete cSCI that closely models this condition in humans. This work directly addresses the current lack of clinically relevant models of cSCI and will thus contribute to improved success in the translation of putative therapies into the clinic.

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“…In addition, the main effect of the so called corticospinal tract is not exerted directly on the motorneurons innervating the muscle, but rather indirectly via a large pool of premotor spinal interneurons (Jankowska 1992;Bortoff and Strick 1993;Isa et al 2006;Alstermark et al 2007). Also, spinal premotor neurons have a divergent innervation to target multiple motorneuron pools (Alstermark et al 1991;Jankowska 1992;Takei and Seki 2010). In other words, all connections, which serve as the infrastructure for neural motor control is naturally synergistic, i.e.…”

Section: The Neuroscience Of Graspingmentioning

confidence: 99%

Human hand modelling: kinematics, dynamics, applications

et al. 2012

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An overview of mathematical modelling of the human hand is given. We consider hand models from a specific background: rather than studying hands for surgical or similar goals, we target at providing a set of tools with which human grasping and manipulation capabilities can be studied, and hand functionality can be described. We do this by investigating the human hand at various levels: (1) at the level of kinematics, focussing on the movement of the bones of the hand, not taking corresponding forces into account; (2) at the musculotendon structure, i.e. by looking at the part of the hand generating the forces and thus inducing the motion; and (3) at the combination of the two, resulting in hand dynam- ics as well as the underlying neurocontrol. Our purpose is to not only provide the reader with an overview of current human hand modelling approaches but also to fill the gaps with recent results and data, thus allowing for an encompassing picture.

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Spinal Interneurons Facilitate Coactivation of Hand Muscles during a Precision Grip Task in Monkeys

Abstract: Grasping is a highly complex movement requiring coordination of a number of hand joints and muscles. In contrast to cortical descending systems, the contribution of the subcortical system for coordinating this higher degree of freedom is largely unknown.

Cited by 105 publications

References 65 publications

Neural basis for hand muscle synergies in the primate spinal cord

Neural basis for hand muscle synergies in the primate spinal cord

Bilateral Contusion-Compression Model of Incomplete Traumatic Cervical Spinal Cord Injury

Human hand modelling: kinematics, dynamics, applications

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