Characterization of Spinal Sensorimotor Network Using Transcutaneous Spinal Stimulation during Voluntary Movement Preparation and Performance

Transcutaneous electrical spinal stimulation (TSS) can be used to selectively activate motor pools based on their anatomical arrangements in the lumbosacral enlargement. These spatial patterns of spinal motor activation may have important clinical implications, especially when there is a need to target specific muscle groups. However, our understanding of the net effects and interplay between the motor pools projecting to agonist and antagonist muscles during the preparation and performance of voluntary movements is still limited. The present study was designed to systematically investigate and differentiate the multi-segmental convergence of supraspinal inputs on the lumbosacral neural network before and during the execution of voluntary leg movements in neurologically intact participants. During the experiments, participants (N = 13) performed isometric (1) knee flexion and (2) extension, as well as (3) plantarflexion and (4) dorsiflexion. TSS consisting of a pair pulse with 50 ms interstimulus interval was delivered over the T12-L1 vertebrae during the muscle contractions, as well as within 50 to 250 ms following the auditory or tactile stimuli, to characterize the temporal profiles of net spinal motor output during movement preparation. Facilitation of evoked motor potentials in the ipsilateral agonists and contralateral antagonists emerged as early as 50 ms following the cue and increased prior to movement onset. These results suggest that the descending drive modulates the activity of the inter-neuronal circuitry within spinal sensorimotor networks in specific, functionally relevant spatiotemporal patterns, which has a direct implication for the characterization of the state of those networks in individuals with neurological conditions.

Short latency stretch reflexes depend on the balance of activity in agonist and antagonist muscles during ballistic elbow movements

The spinal stretch reflex is a fundamental building block of motor function, modulating sensitivity across tasks to augment volitional control. Stretch reflex sensitivity can vary continuously during movement and changes between movement and posture. While there have been many demonstrations of reflex modulation and investigations into the underlying mechanisms, there have been few attempts to provide simple, quantitative descriptions of the relationship between the volitional control and stretch reflex sensitivity throughout tasks that require the coordinated activity of several muscles. Here we develop such a description and use it to test the hypothesis that the modulation of stretch reflex sensitivity during movement can be explained by the balance of activity within the relevant agonist and antagonist muscles better than by the activity only in the muscle homonymous with the elicited reflex. We applied continuous pseudo-random perturbations of elbow angle as subjects completed approximately 500 movements in elbow flexion and extension. Measurements were averaged across the repeated movements to obtain continuous estimates of stretch reflex amplitude and background muscle activity. We also ran a control experiment on a subset of subjects performing postural tasks at muscle activity levels matched to those measured in the movement task. For both experiments, we assessed the relationship between background activity in the agonist and antagonist muscles controlling elbow movement and the stretch reflexes elicited in them. We found that modulation in the stretch reflexes during movement can be described by modulation of the background activity in the agonist and antagonist muscles, and that models incorporating agonists and antagonists are significantly better than those considering only the homonymous muscle. Increases in agonist muscle activity enhanced stretch reflex sensitivity whereas increases in antagonist activity suppressed reflex activity. Surprisingly, the magnitude of these effects was similar, suggesting a balance of control between agonists and antagonist that is very different than the dominance of sensitivity to agonist activity during postural tasks. This greater relative sensitivity to antagonist background activity during movement is due to a large decrease in sensitivity to homonymous muscle activity during movement rather than substantial changes in the influence of antagonist muscle activity.

When Antagonist Muscles at the Ankle Interfere with Maximal Voluntary Contraction under Isometric and Anisometric Conditions

Purpose: While resultant maximal voluntary contraction (MVC) is commonly used to assess muscular performance, the simultaneous activation of antagonist muscles could dramatically underestimate the strength of the agonist muscles. While quantification of antagonist torque has been performed in plantar- (PF) and dorsi-flexion (DF) joint in isometric conditions, it has yet to be determined in anisometric (concentric and eccentric) conditions. Methods: The experiment was performed in 9 participants through 2 sessions (reliability). The MVCs in DF and PF were measured in isometric, concentric and eccentric conditions (10°.s-1). Electromyographic (EMG) activities from the soleus, gastrocnemius medialis and lateralis, and tibialis anterior muscles were simultaneously recorded. The EMG biofeedback method was used to quantify antagonist torque, where participants were asked to maintain a level of EMG activity, corresponding to antagonist EMG activity and related to the muscle contraction type, according to a visual EMG bio-feedback displayed on a screen. Results: Resultant torque significantly underestimated agonist torque in DF MVC (30-65%) and to a lesser extent in PF MVC (3%). Triceps surae antagonist torque was significantly modified with muscle contraction type, showing higher antagonist torque in isometric (29 Nm) than eccentric (23 Nm, p < 0.001) and concentric (14 Nm, p < 0.001) conditions and resulting in modification of the DF MVC torque-velocity shape. The difference between DF eccentric and concentric MVC was attenuated when considered agonist torque (12%) rather than resultant torque (45%). Conclusion: Estimation of the antagonist torque in isometric or anisometric condition brings new insights to assessment of muscular performance and could result in costly misinterpretation in strength training and/or rehabilitation programs.

Proximal and distal spinal neurons innervating multiple synergist and antagonist motor pools

Motoneurons control muscle contractions, and their recruitment by premotor circuits is tuned to produce accurate motor behaviours. To understand how these circuits coordinate movement across and between joints, it is necessary to understand whether spinal neurons pre-synaptic to motor pools have divergent projections to more than one motoneuron population. Here, we used modified rabies virus tracing in mice to investigate premotor INs projecting to synergist flexor or extensor motoneurons, as well as those projecting to antagonist pairs of muscles controlling the ankle joint. We show that similar proportions of premotor neurons diverge to synergist and antagonist motor pools. Divergent premotor neurons were seen throughout the spinal cord, with decreasing numbers but increasing proportion with distance from the hindlimb enlargement. In the cervical cord, divergent long descending propriospinal neurons were found in contralateral lamina VIII, had large somata, were neither glycinergic, nor cholinergic, and projected to both lumbar and cervical motoneurons. We conclude that distributed spinal premotor neurons coordinate activity across multiple motor pools and that there are spinal neurons mediating co-contraction of antagonist muscles.

Antagonist surface electromyogram decomposition and the case of the missing motor units

Reece & Herda (2021) reported that an antagonist muscle exhibited an organized motor unit (MU) recruitment scheme during isometric elbow flexion contractions. This control scheme, however, differed from the typical MU control scheme in that MU firing rates did not change between force levels (40% and 70% MVC) in the triceps brachii when it acted as an antagonist to isometric elbow flexion. Here we suggest technological considerations with evidence that may have affected these findings. Additionally, we highlight how this paper offers a promising starting point from which further insight into antagonist MU behaviour can be gathered non-invasively, and suggest future research directions to improve our understanding of MU activity of antagonist muscles in the upper limb.

Costs of position, velocity, and force requirements in optimal control induce triphasic muscle activation during reaching movement

The nervous system activates a pair of agonist and antagonist muscles to determine the muscle activation pattern for a desired movement. Although there is a problem with redundancy, it is solved immediately, and movements are generated with characteristic muscle activation patterns in which antagonistic muscle pairs show alternate bursts with a triphasic shape. To investigate the requirements for deriving this pattern, this study simulated arm movement numerically by adopting a musculoskeletal arm model and an optimal control. The simulation reproduced the triphasic electromyogram (EMG) pattern observed in a reaching movement using a cost function that considered three terms: end-point position, velocity, and force required; the function minimised neural input. The first, second, and third bursts of muscle activity were generated by the cost terms of position, velocity, and force, respectively. Thus, we concluded that the costs of position, velocity, and force requirements in optimal control can induce triphasic EMG patterns. Therefore, we suggest that the nervous system may control the body by using an optimal control mechanism that adopts the costs of position, velocity, and force required; these costs serve to initiate, decelerate, and stabilise movement, respectively.

Temporal Dynamics of Corticomuscular Coherence Reflects Alteration of the Central Mechanisms of Neural Motor Control in Post-Stroke Patients

The neural control of muscular activity during a voluntary movement implies a continuous updating of a mix of afferent and efferent information. Corticomuscular coherence (CMC) is a powerful tool to explore the interactions between the motor cortex and the muscles involved in movement realization. The comparison of the temporal dynamics of CMC between healthy subjects and post-stroke patients could provide new insights into the question of how agonist and antagonist muscles are controlled related to motor performance during active voluntary movements. We recorded scalp electroencephalography activity, electromyography signals from agonist and antagonist muscles, and upper limb kinematics in eight healthy subjects and seventeen chronic post-stroke patients during twenty repeated voluntary elbow extensions and explored whether the modulation of the temporal dynamics of CMC could contribute to motor function impairment. Concomitantly with the alteration of elbow extension kinematics in post-stroke patients, dynamic CMC analysis showed a continuous CMC in both agonist and antagonist muscles during movement and highlighted that instantaneous CMC in antagonist muscles was higher for post-stroke patients compared to controls during the acceleration phase of elbow extension movement. In relation to motor control theories, our findings suggest that CMC could be involved in the online control of voluntary movement through the continuous integration of sensorimotor information. Moreover, specific alterations of CMC in antagonist muscles could reflect central command alterations of the selectivity in post-stroke patients.

Isometric agonist and antagonist muscle activation interacts differently with 140 Hz tACS aftereffects at different intensities

Introduction: 1) During tES, increasing intracellular Ca2+ levels beyond those needed for inducing LTP may collapse aftereffects. 2) State-dependent plastic aftereffects are reduced when applied during muscle activation as compared to rest. 3) Cortical surround inhibition by antagonistic muscle activation inhibits the center-innervated agonist. Objectives: To determine the interaction of state dependency of tACS aftereffects at rest and under activation of agonist and antagonist muscles during stimulation with different intensities. Methods: In thirteen healthy participants, we measured MEP amplitudes before and after applying tACS at 140 Hz over the motor cortex in nine single-blinded sessions using sham, 1 mA and 2 mA stimulation intensities during rest and activation of agonist and antagonist muscles. Results: During rest, only 1 mA tACS produced a significant MEP increase, while the 2 mA stimulation produced no significant MEP size shift. During agonist activation 1 mA did not induce MEP changes, after 2 mA first a decrease and later an increase of MEPs were observed. Antagonist activation under sham tACS led to an inhibition, which was restored to baseline by 1 and 2 mA tACS. Conclusions: Increasing stimulation intensity beyond 1 mA does not increase excitability, compatible with too strong intracellular Ca2+increase. Antagonist innervation leads to MEP inhibition supporting the concept of surround inhibition, which can be overcome by tACS at both intensities. During agonist innervation a tACS dose dependent relationship exists. Significance: Our results integrate concepts of "leaky membranes" under activation, surround inhibition, intracellular Ca2+ increase and their role in the aftereffects of tACS.