Population spatiotemporal dynamics of spinal intermediate zone interneurons during air-stepping in adult spinal cats

AuYong, Nicholas; Ollivier-Lanvin, Karen; Lemay, Michel

doi:10.1152/jn.00258.2011

Cited by 15 publications

(18 citation statements)

References 60 publications

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“…The effect of methoxamine administration on each dependent variable was determined using separate linear mixed models. Independent variables in the model included drug (administered/not administered) and animal (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20). Drug was included in the model as a fixed, repeated factor, and animal was included as a random factor with a random intercept and random slope over the effect of drug.…”

Section: Discussionmentioning

confidence: 99%

Exogenous neuromodulation of spinal neurons induces beta-band coherence during self-sustained discharge of hind limb motor unit populations

Thompson

Johnson

Negro

et al. 2019

Journal of Applied Physiology

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The spontaneous or self-sustained discharge of spinal motoneurons can be observed in both animals and humans. Although the origins of this self-sustained discharge are not fully known, it can be generated by activation of persistent inward currents intrinsic to the motoneuron. If self-sustained discharge is generated exclusively through this intrinsic mechanism, the discharge of individual motor units will be relatively independent of one another. Alternatively, if increased activation of premotor circuits underlies this prolonged discharge of spinal motoneurons, we would expect correlated activity among motoneurons. Our aim is to assess potential synaptic drive by quantifying coherence during self-sustained discharge of spinal motoneurons. Electromyographic activity was collected from 20 decerebrate animals using a 64-channel electrode grid placed on the isolated soleus muscle before and following intrathecal administration of methoxamine, a selective α1-noradrenergic agonist. Sustained muscle activity was recorded and decomposed into the discharge times of ~10–30 concurrently active individual motor units. Consistent with previous reports, the self-sustained discharge of motor units occurred at low mean discharge rates with low-interspike variability. Before methoxamine administration, significant low-frequency coherence (<2 Hz) was observed, while minimal coherence was observed within higher frequency bands. Following intrathecal administration of methoxamine, increases in motor unit discharge rates and strong coherence in both the low-frequency and 15- to 30-Hz beta bands were observed. These data demonstrate beta-band coherence among motor units can be observed through noncortical mechanisms and that neuromodulation of spinal/brainstem neurons greatly influences coherent discharge within spinal motor pools. NEW & NOTEWORTHY The correlated discharge of spinal motoneurons is often used to describe the input to the motor pool. We demonstrate spinal/brainstem neurons devoid of cortical input can generate correlated motor unit discharge in the 15- to 30-Hz beta band, which is amplified through neuromodulation. Activity in the beta band is often ascribed to cortical drive in humans; however, these data demonstrate the capability of the mammalian segmental motor system to generate and modulate this coherent state of motor unit discharge.

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Section: Discussionmentioning

confidence: 99%

Exogenous neuromodulation of spinal neurons induces beta-band coherence during self-sustained discharge of hind limb motor unit populations

Thompson

Johnson

Negro

et al. 2019

Journal of Applied Physiology

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“…Rotational dynamics has been observed in the motor cortex and elsewhere [9][10][11] , but it has not been described for spinal circuits previously. Nevertheless, indications can be found as wide phase-distributions in the scarce literature on spinal population recordings 6,[12][13][14] . Fig.…”

Section: Rotation In Spinal Motor Circuitsmentioning

confidence: 99%

Movement is governed by rotational population dynamics in spinal motor networks

Lindén

Petersen

Vestergaard

et al. 2021

Preprint

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Although the nervous system is elegantly orchestrating movements, the underlying neural principles remain unknown. Since flexor- and extensor-muscles alternate during movements like walking, it is often assumed that the responsible neural circuitry is similarly alternating in opposition. Here, we present ensemble-recordings of neurons in the turtle lumbar spinal cord that indicate that, rather than alternation, the population is performing a "rotation" in neural space, i.e. the neural activity is cycling through all phases continuously during the rhythmic behavior. The radius of rotation correlates with the intended muscle force. Since existing models of spinal motor control offer inadequate explanation of this dynamics, we propose a new theory of neural generation of movement from which rotation and other unresolved issues, such as speed regulation, force control, and multi-functionalism, are conveniently explained.

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“…; Auyong et al. ), evidence for its existence has been observed in frogs (Saltiel et al. ), rodents (Cazalets ), and cats (Cuellar et al.…”

Section: Introductionmentioning

confidence: 98%

Motor module activation sequence and topography in the spinal cord during air‐stepping in human: Insights into the traveling wave in spinal locomotor circuits

Yokoyama

Hagio

Ogawa

et al. 2017

Physiological Reports

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Coordinated locomotor muscle activity is generated by the spinal central pattern generators (CPGs), which are modulated by peripheral and supraspinal inputs. The CPGs would consist of multiple motor modules generating basic muscle activity, which are distributed rostrocaudally along the spinal cord. To activate the motor modules in proper sequence, rostrocaudally traveling waves of activation in the spinal cord are important mechanisms in the CPGs. The traveling waves of activation have been observed in nonhuman vertebrates. However, they have not yet been confirmed during human locomotion. Although, rostrocaudal wave‐like activations in the spinal cord were observed during walking in humans in a previous study, the propagation shifted rostrally toward the upper lumbar segments at foot contact. Here, using an air stepping task to remove the foot‐contact interactions, we examined whether the traveling wave mechanism exists in the human spinal circuits based on the activation sequence of motor modules and their topography. We measured electromyographic activity of lower leg muscles during the air‐stepping task. Then, we extracted motor modules (i.e., basic patterns of sets of muscle activations: muscle synergies) from the measured muscle activities using nonnegative matrix factorization method. Next, we reconstructed motoneuron (MN) activity from each module activity based on myotomal charts. We identified four types of motor modules from muscle activities during the air‐stepping task. Each motor module represented different sets of synergistic muscle activations. MN clusters innervating each motor module were sequentially activated from the rostral to caudal region in the spinal cord, from the initial flexion to the last extension phase during air‐stepping. The rostrocaudally sequential activation of MN clusters suggests the possibility that rostrocaudally traveling waves exist in human locomotor spinal circuits. The present results advance the understanding of human locomotor control mechanisms, and provide important insights into the evolution of locomotor networks in vertebrates.

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Population spatiotemporal dynamics of spinal intermediate zone interneurons during air-stepping in adult spinal cats

Cited by 15 publications

References 60 publications

Exogenous neuromodulation of spinal neurons induces beta-band coherence during self-sustained discharge of hind limb motor unit populations

Exogenous neuromodulation of spinal neurons induces beta-band coherence during self-sustained discharge of hind limb motor unit populations

Movement is governed by rotational population dynamics in spinal motor networks

Motor module activation sequence and topography in the spinal cord during air‐stepping in human: Insights into the traveling wave in spinal locomotor circuits

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