Transcutaneous and epidural electrical spinal cord stimulation techniques are becoming more valuable as electrophysiological and clinical tools. Recently, remarkable recovery of the upper limb ...sensorimotor function during cervical spinal stimulation was demonstrated. In the present study, we sought to elucidate the neural mechanisms underlying the effects of transcutaneous spinal cord stimulation (tSCS) of the cervical spine. We hypothesized that cervical tSCS can be used to selectively activate the sensory route entering the spinal cord and transsynaptically converge on upper limb motor pools. To test this hypothesis, we applied cervical tSCS using paired stimuli (homosynaptic depression) and during passive muscle stretching of the wrist flexor (presynaptic inhibition via Ia afferents), voluntary hand muscle contraction (descending facilitation of motoneuron pool), and muscle-tendon vibration of the wrist (presynaptic inhibition via afferent occlusion). Our results demonstrate significant inhibition of the second evoked response during paired stimulus delivery, inhibition of responses during passive muscle stretching and muscle-tendon vibration, and facilitation during voluntary muscle contraction, which share similarities with responses evoked during lumbosacral tSCS. These results indicate that the route of the stimulation current transmission passes via afferents in the dorsal roots through the spinal cord to activate the motor pools and potentially interneuronal networks projecting to upper limb muscles. Using a novel stimulation paradigm, our study is the first to present evidence of the sensory neuronal pathway of the cervical tSCS propagation. Overall, our work demonstrates the utility and sensitivity of cervical tSCS to engage the sensory pathway projecting to the upper limbs.
Despite therapeutic effects that have been demonstrated previously using noninvasive cervical spinal stimulation, it has been unclear whether, and to what degree, the stimulation can activate the sensory afferent system. Our study presents evidence that cervical transcutaneous spinal cord stimulation can engage the sensory pathways and transsynaptically converge on motor pools projecting to upper limb muscles, demonstrating the utility and sensitivity of cervical spinal stimulation for electrophysiological assessments and neurorehabilitation.
•Upper-limb muscle contractions facilitated corticospinal, but not subcortical neural circuits of the remote trunk muscles.•Trunk muscle contractions facilitated both corticospinal and subcortical ...neural circuits of the remote upper-limb muscles.•Corticospinal neurons may have complex outputs to multiple muscles which interact within cortical and spinal circuits.
Activities of daily living require simultaneous and coordinated activation of trunk and upper-limb segments, which involves complex interlimb interaction within the central nervous system. Although many studies have reported associations between activity of trunk and limb muscles during functional tasks, evidence on cortical and subcortical contributions to trunk-limb neural interactions is still not fully clear. Therefore, the aim of this study was to examine interactions between trunk and upper-limb muscles in the: (i) corticospinal circuits by using motor evoked potential (MEP) elicited through transcranial magnetic stimulation; and (ii) subcortical circuits by using cervicomedullary motor evoked potential (CMEP) elicited through cervicomedullary junction magnetic stimulation. Responses were evoked in the erector spinae (trunk) and flexor carpi radialis (upper-limb) muscles in twelve able-bodied individuals: (1) while participants were relaxed; (2) during trunk muscle contractions while arms were at rest; and (3) during upper-limb muscle contractions while the trunk was at rest. Our results showed that trunk muscle CMEP responses were not affected by upper-limb muscle contractions, while MEP responses were modulated. This indicates that at least the subcortical circuits may not attribute to facilitation of the trunk muscles during upper-limb contractions. On the other hand, in the upper-limb muscles, both CMEP and MEP responses were modulated during trunk contractions. These results indicate that cortical and subcortical mechanisms attributed to facilitation of upper-limb muscles during trunk contractions. In conclusion, our study demonstrated evidence that trunk-limb neural interactions may be attributed to cortical and/or subcortical mechanisms depending on the contracted muscle.
It is well known that contracting the upper limbs can affect spinal reflexes of the lower limb muscle, via intraneuronal networks within the central nervous system. However, it remains unknown ...whether neuromuscular electrical stimulation (NMES), which can generate muscle contractions without central commands from the cortex, can also play a role in such inter-limb facilitation. Therefore, the objective of this study was to compare the effects of unilateral upper limb contractions using NMES and voluntary unilateral upper limb contractions on the inter-limb spinal reflex facilitation in the lower limb muscles. Spinal reflex excitability was assessed using transcutaneous spinal cord stimulation (tSCS) to elicit responses bilaterally in multiple lower limb muscles, including ankle and thigh muscles. Five interventions were applied on the right wrist flexors for 70 s: (1) sensory-level NMES; (2) motor-level NMES; (3) voluntary contraction; (4) voluntary contraction and sensory-level NMES; (5) voluntary contraction and motor-level NMES. Results showed that spinal reflex excitability of ankle muscles was facilitated bilaterally during voluntary contraction of the upper limb unilaterally and that voluntary contraction with motor-level NMES had similar effects as just contracting voluntarily. Meanwhile, motor-level NMES facilitated contralateral thigh muscles, and sensory-level NMES had no effect. Overall, our results suggest that inter-limb facilitation effect of spinal reflex excitability in lower limb muscles depends, to a larger extent, on the presence of the central commands from the cortex during voluntary contractions. However, peripheral input generated by muscle contractions using NMES might have effects on the spinal reflex excitability of inter-limb muscles via spinal intraneuronal networks.
Ankle dorsiflexion force control is essential for performing daily living activities. However, the involvement of the corticospinal pathway during different ankle dorsiflexion tasks is not well ...understood. The objective of this study was to compare the corticospinal excitability during: (1) unilateral and bilateral; and (2) ballistic and tonic ankle dorsiflexion force control. Fifteen healthy young adults (age: 25.2 ± 2.8 years) participated in this study. Participants performed unilateral and bilateral isometric ankle dorsiflexion force-control tasks, which required matching a visual target (10% of maximal effort) as quickly and precisely as possible during ballistic and tonic contractions. Transcranial magnetic stimulation (TMS) was applied over the primary motor cortex to elicit motor-evoked potentials (MEPs) from the right tibialis anterior during: (i) pre-contraction phase; (ii) ascending contraction phase; (iii) plateau phase (tonic tasks only); and (iv) resting phase (control). Peak-to-peak MEP amplitude was computed to compare the corticospinal excitability during each experimental condition. MEP amplitudes significantly increased during unilateral contraction compared to bilateral contraction in the pre-contraction phase. There were no significant differences in the MEP amplitudes between the ballistic tasks and tonic tasks in any parts of the contraction phase. Although different strategies are required during ballistic and tonic contractions, the extent of corticospinal involvement appears to be similar. This could be because both tasks enhance the preparation for precise force control. Furthermore, our results suggest that unilateral muscle contractions may largely facilitate the central nervous system during movement preparation for unilateral force control compared to bilateral muscle contractions.
Neural interactions between upper and lower limbs underlie motor coordination in humans. Specifically, upper limb voluntary muscle contraction can facilitate spinal and corticospinal excitability of ...the lower limb muscles. However, little remains known on the involvement of somatosensory information in arm‐leg neural interactions. Here, we investigated effects of voluntary and electrically induced wrist flexion on corticospinal excitability and somatosensory information processing of the lower limbs. In Experiment 1, we measured transcranial magnetic stimulation (TMS)‐evoked motor evoked potentials (MEPs) of the resting soleus (SOL) muscle at rest or during voluntary or neuromuscular electrical stimulation (NMES)‐induced wrist flexion. The wrist flexion force was matched to 10% of the maximum voluntary contraction (MVC). We found that SOL MEPs were significantly increased during voluntary, but not NMES‐induced, wrist flexion, compared to the rest (P < .001). In Experiment 2, we examined somatosensory evoked potentials (SEPs) following tibial nerve stimulation under the same conditions. The results showed that SEPs were unchanged during both voluntary and NMES‐induced wrist flexion. In Experiment 3, we examined the modulation of SEPs during 10%, 20% and 30% MVC voluntary wrist flexion. During 30% MVC voluntary wrist flexion, P50‐N70 SEP component was significantly attenuated compared to the rest (P = .003). Our results propose that the somatosensory information generated by NMES‐induced upper limb muscle contractions may have a limited effect on corticospinal excitability and somatosensory information processing of the lower limbs. However, voluntary wrist flexion modulated corticospinal excitability and somatosensory information processing of the lower limbs via motor areas.
Corticospinal excitability of the lower limb muscle was facilitated during voluntary, but not NMES‐induced, upper limb muscle contractions. Responses to somatosensory stimulation of the lower limb were unchanged during either voluntary or NMES‐induced upper limb muscle contractions. When voluntary contraction intensity was increased, responses to somatosensory stimulation of the lower limb were partially attenuated.
•Interaction of trunk, limbs and jaw in the corticospinal pathway was examined.•Trunk muscles contraction modulated corticospinal excitability of limb muscles.•Limbs muscle contraction modulated ...corticospinal excitability of trunk muscle.•Results showed evidence for trunk-limb interaction in the corticospinal pathway.
In humans, trunk muscles have an essential role in postural control as well as walking. However, little is known about the mechanisms of interaction with different muscles, especially related to how trunk muscles interact with the limbs. Contraction of muscles can modulate the corticospinal excitability not only of the contracted muscle, but also of other muscles even in the remote segments of the body. However, “remote effect” mechanism has only been examined for inter-limb interactions. The aim of our current study was to test if there are trunk-limb interactions in the corticospinal pathways. We examined corticospinal excitability of: (a) trunk muscles at rest when hands, legs and jaw muscles were contracted and; (b) hand, leg, and jaw muscles at rest when trunk muscles were contracted. We measured motor evoked potentials elicited using transcranial magnetic stimulation in the rectus abdominis, flexor digitorum superficialis, masseter, tibialis anterior muscles under the following experimental conditions: (1) participants remained relaxed (Rest); (2) during trunk contraction (Trunk); (3) during bilateral hand clenching (Hands); (4) during jaw clenching (Jaw); and (5) during bilateral ankle dorsiflexion (Legs). Each condition was performed at three different stimulation intensities and conditions were randomized between participants. We found that voluntary contraction of trunk muscle facilitated the corticospinal excitability of upper-limb and lower-limb muscles during rest state. Furthermore, voluntary contraction of upper-limb muscle also facilitated the corticospinal excitability of trunk muscles during rest state. Overall, these results suggest the existence of trunk-limb interaction in the corticospinal pathway, which is likely depended on proximity of the trunk and limb representation in the motor cortex.
Non-invasive theta burst stimulation (TBS) can elicit facilitatory or inhibitory changes in the central nervous system when applied intermittently (iTBS) or continuously (cTBS). Conversely, ...neuromuscular electrical stimulation (NMES) can activate the muscles to send a sensory volley, which is also known to affect the excitability of the central nervous system. We investigated whether cortical iTBS (facilitatory) or cTBS (inhibitory) priming can affect subsequent NMES-induced corticospinal excitability. A total of six interventions were tested, each with 11 able-bodied participants: cortical priming followed by NMES (iTBS + NMES and cTBS + NMES), NMES only (iTBS
sham
+ NMES and cTBS
sham
+ NMES), and cortical priming only (iTBS + rest and cTBS + rest). After iTBS or cTBS priming, NMES was used to activate right extensor capri radialis (ECR) muscle intermittently for 10 min (5 s ON/5 s OFF). Single-pulse transcranial magnetic stimulation motor evoked potentials (MEPs) and maximum motor response (
M
max
) elicited by radial nerve stimulation were compared before and after each intervention for 30 min. Our results showed that associative facilitatory iTBS + NMES intervention elicited greater MEP facilitation that lasted for at least 30 min after the intervention, while none of the interventions alone were effective to produce effects. We conclude that facilitatory iTBS priming can make the central nervous system more susceptible to changes elicited by NMES through sensory recruitment to enhance facilitation of corticospinal plasticity, while cTBS inhibitory priming efficacy could not be confirmed.
The rambling and trembling analysis separates the center of pressure (COP) fluctuations into two components: rambling (supraspinal contribution) and trembling (muscle stiffness / reflexive properties ...contribution). We examined whether the trembling component is correlated to the contractile properties (muscle stiffness and contraction time) of lower limb superficial skeletal muscles to experimentally test the rambling and trembling hypothesis. We hypothesized that muscle stiffness and contraction time, would be: (a) more correlated with; and (b) have a greater impact on the trembling component compared to the rambling component. Thirty-two healthy young adults were recruited for the study and tensiomyography was used to assess mechanical muscle responses to a single electrical stimulus to calculate muscle stiffness and contraction time based on radial muscle belly displacement measurements of lower limb muscles unilaterally. Moreover, upright postural control was assessed using a force plate to record ground reaction forces and moments and calculate the COP fluctuations during two 30 seconds trials. From the COP fluctuations, rambling and trembling time series were extracted, and all fluctuation time series were described using a number of different time-domain and frequency-domain parameters in both the anterior-posterior and medial-lateral directions. Our results demonstrated that both muscle stiffness and contraction time were moderately correlated with time-domain and frequency-domain parameters of the trembling component, as compared with those of the rambling component which was not as well correlated. Moreover, they also predicted the trembling component better. Overall, these results imply that postural control during quiet stance is, in part, related to intrinsic muscle stiffness in the lower extremities. Moreover, we showed that the rambling and trembling hypothesis is effective in separating postural sway fluctuations during upright posture to extract the contributions of muscle stiffness / reflexive properties (trembling), and likely the supraspinal contribution (rambling).
We investigated whether bilateral lower-limb control and leg dominance affect force control ability in 15 healthy young adults (9 males and 6 females, age =26.8 ± 4.1 years). Participants performed ...isometric ankle dorsiflexion force control tasks, matching a visual target (10% of maximal effort) as quickly and precisely as possible in ballistic and tonic tasks. Performance was evaluated using force error, force steadiness, amount of muscle activity of the tibialis anterior, and response time characteristics. Results showed no significant effects of leg dominance during both ballistic and tonic tasks, while bilateral condition resulted in significantly larger error, less force steadiness, compared to unilateral condition, and only during the tonic task. Consequently, bilateral control, specifically in tasks utilizing feedback control (i.e., tonic task) might affect force control ability, possibly because of the interhemispheric inhibition to meet bilateral task complexity and integrate afferent bilateral sensory information from both right and left legs.
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