Few patients recover full hand dexterity after an acquired brain injury such as stroke. Repetitive somatosensory electrical stimulation (SES) is a promising method to promote recovery of hand function. However, studies using SES have largely focused on gross motor function; it remains unclear if it can modulate distal hand functions such as finger individuation.
Eight participants with a history of acquired brain injury and distal upper limb motor impairments received a single two-hour session of SES using transcutaneous electrical nerve stimulation. Pre- and post-intervention assessments consisted of the Action Research Arm Test (ARAT), finger fractionation, pinch force, and the modified Ashworth scale (MAS), along with resting-state EEG monitoring.
Sensory threshold somatosensory electrical stimulation (SES) is a promising therapeutic modality for targeting hand motor recovery . It is known to be a powerful tool to focally modulate sensorimotor cortices in both healthy and chronic stroke participants [5,6,7,8]. Devices such as transcutaneous nerve stimulation (TENS) units can deliver SES and are commercially available, inexpensive, low risk, and easily applied in the home setting . Previous studies have demonstrated short-term and long-term improvements in hand function after SES [5, 10,11,12,13,14,15]. However, the effect of SES on regaining the ability to selectively move a given digit independently from other digits (i.e. finger fractionation) has not been investigated. Poor finger individualization is an important therapeutic target because it is commonly present even after substantial recovery and may account for chronic hand dysfunction . Further, it is unclear if SES is associated with compensatory or restorative mechanisms. Prior studies have largely relied on relatively subjective clinical evaluations of impairment, such as the Fugl-Meyer Assessment, or timed and task-based assessments, such as the Jebson-Taylor Hand Function Test. Biomechanical analyses, on the other hand, can provide important objective and quantitative evidence of improvement in neurologic function and normative motor control [17, 18]. Therefore, we aimed to determine not only the functional effects, but also the kinematic effects, of SES on chronic hand dysfunction.
a Schematic representation of the method used for calculating the FCI. The participant is instructed to flex only the index finger as much as possible without flexing the other digits. b FCI is defined mathematically as the angle traversed by the middle finger (digit A) divided by the angle tranversed by the index finger (digit B) relative to the horizontal starting position. c Statistically significant change in mean fractionation from baseline to immediately after peripheral nerve stimulation. Fractionation improvement is indicated by a decrease in finger coupling index (FCI)
TENS was performed using a commercially available device (ProStim, Alimed Inc., Dedham, Massachusetts, USA). One pair of 2 × 3.5 in. rectangular electrodes (Vermed ChroniCare TENS Electrodes, Vermed, Buffalo, NY, USA) were placed on one aspect of the forearm to simultaneously stimulate both median and ulnar nerves, while a second pair of round 2 in. diameter electrodes were placed on the lateral aspect of the forearm to stimulate the radial nerve. (Additional file 1: Figure S2) Optimal positions to stimulate the ulnar, median and radial nerves of the paretic hand were determined by using standard localization technique [26, 25]. Sensory thresholds (minimum intensity of stimulation) at which subjects report paresthesias in each nerve territory were determined. Stimulus intensity was further increased and adjusted until subjects reported strong paresthesias in the absence of pain and visible muscle contractions. The mean stimulation intensity was 5.3 mA (19% above mean sensory threshold) for the radial nerve and 5.8 mA (29% above mean sensory threshold) for the median/ulnar nerves. Bursts of electrical stimulation at 10 Hz (100 microsecond pulse width duration) were delivered to all nerves simultaneously for 2 h [5, 10, 12,13,14,15, 18]. During the stimulation period, the affected hand was at rest while participants read or viewed a film.
Results of kinematic and clinical outcome measurements are presented in Table 2. Mean scores were significantly improved after peripheral nerve stimulation for measures including ARAT total score, overall ARAT completion time, ARAT pinch tasks subset completion time, finger coupling index, and MAS. The mean change in ARAT score was 1.5 points change (or 3.75% improvement) after one session of SES (p
Our primary results showed that a single two-hour session of SES resulted in statistically significant improvements in functional measurements as well as finger kinematics in individuals with chronic acquired brain injury. Improvements were found in the domains of activity (i.e. ARAT) and impairment (i.e. pinch strength, spasticity, and finger fractionation). A statistically significant improvement was detected in the mean ARAT score after only one session of SES. This finding is broadly consistent with similar studies of the effects of SES on hand function in stroke patients [3, 5, 15, 19, 31]. One particular study using the ARAT, however, did not find any change after SES. It was determined to be largely due to a ceiling effect . For example, their participants averaged a higher baseline ARAT score than the participants in the present study. While the change in ARAT score was small in magnitude, it may be of clinical relevance; larger or additive effects have been demonstrated with multiple stimulation sessions and in combination with motor training [32, 33].
The relationship between SES and recovery of individuated finger movements has not been investigated in previous studies. Past studies mainly focused on functional measurements as outcomes, such as the Jebson-Taylor Hand Function Test, or on relatively subjective evaluations of impairment, such as the Fugl-Meyer Assessment, to determine the efficacy of SES [5, 10, 15, 19, 31]. Combining functional clinical evaluations with kinematic measurements of finger fractionation is one strategy we implemented to distinguish between functional improvements solely related to compensatory changes versus recovery of impairments. For the purpose of this study, we defined treatment-induced motor recovery as a relative improvement in finger fractionation ability after peripheral nerve stimulation. Our finding here of normalized finger fractionation kinematics suggests that SES can modulate the neural control of finger dexterity. This observation is consistent with a prior study demonstrating immediate improvement in index finger and hand tapping frequency after a single 2-h session of SES.  Interestingly, the ARAT total score improvement was specifically attributable to improved performance in pinch tasks rather than performance of grip, grasp, or proximal tasks. This indicates that SES may have a highly specific or greater effect on tasks that require relatively more finger individuation. However, findings of improvements in peak velocity of the wrist during reach-to-grasp tasks after SES have also been reported.  Although the differential effect of SES on the various aspects of upper limb function needs further evaluation, the findings taken together underline the importance of emphasizing recovery of finger dexterity to facilitate meaningful and measurable functional improvements.
The specific mechanism for increased fractionation ability after SES is unclear. Prior research suggests that SES affects complex motor skill performance by re-organization and altered excitability of the sensorimotor cortex. Neuroanatomical, electrophysiological, and imaging data revealed that unilateral electrical stimulation, including SES, can activate the contralateral S1 and S2 bilaterally [34,35,36,37,38]. Direct connections between Brodmann areas 1 and 2 of S1 and M1, and S2 and M1 could provide a neuroanatomical basis for the observed effects [39,40,41,42,43]. Furthermore, when patients with pure motor lacunar strokes have interrupted corticospinal projections at a subcortical location, the remaining descending pathways mediating voluntary movement are unable to produce selective patterns of muscle activation required for finger individuation tasks.  This underlines the importance of motor cortex output for the orchestration of individuated finger movements. Studies have shown no effects on peripheral nerve M-wave and spinal cord excitability (H waves) with SES, further suggesting that the changes in excitability most likely occur at the level of the cortex. [44, 45]
It has been proposed that finger individuation is a result of not only the voluntary movement of one digit but also the inhibition of digits intended to remain stationary . One study using high frequency SES found a reduction in motor evoked potential (MEP) from the muscle stimulated and an increased MEP from the antagonist muscle . A more recent study found increased MEP with supramotor threshold stimulation and reduced MEPs with SES . Although these results cannot be directly compared to our findings because the stimulation parameters and conditions were dissimilar, they illustrate the complexity of the parameter-dependent effects of SES that can be both facilitatory as well as inhibitory. Therefore, it is plausible that SES improves motor control during finger individuation tasks by modulating cortical excitability and inhibiting inappropriate antagonist and agonist muscle co-contractions, a hypothesis in need of further exploration. The plausible neural correlates underlying the proposed corticomotor excitability changes are addressed in the following paragraph based on our EEG results.
In summary, we demonstrated the feasibility of using a wearable EEG system with 8 channels to monitor and serve as a biomarker of treatment response. However, using a higher resolution EEG system with a greater number of channels may be more informative, albeit more cumbersome to apply. Given the small sample size, it is unclear whether inhomogeneity of baseline sensory impairments would impact individual responses to SES. Investigations into the impact of sensory deficits and generalizability of findings in a larger patient population is warranted. Future studies will also need to address other potential limitations of this pilot study, including the need for a randomized, controlled study design, monitoring of long-term effects of SES, varying dosing and stimulation parameters to determine their effects on EEG, and explorations into the mechanisms for the effects of SES on complex motor skills. 2b1af7f3a8