Effects of transcutaneous spinal stimulation on spatiotemporal cortical activation patterns: a proof-of-concept EEG study.

Objective.Transcutaneous spinal cord stimulation (TSS) has been shown to be a promising non-invasive alternative to epidural spinal cord stimulation for improving outcomes of people with spinal cord injury (SCI). However, studies on the effects of TSS on cortical activation are limited. Our objectives were to evaluate the spatiotemporal effects of TSS on brain activity, and determine changes in functional connectivity under several different stimulation conditions. As a control, we also assessed the effects of functional electrical stimulation (FES) on cortical activity.Approach. Non-invasive scalp electroencephalography (EEG) was recorded during TSS or FES while five neurologically intact participants performed one of three lower-limb tasks while in the supine position: (1) A no contraction control task, (2) a rhythmic contraction task, or (3) a tonic contraction task. After EEG denoising and segmentation, independent components (ICs) were clustered across subjects to characterize sensorimotor networks in the time and frequency domains. ICs of the event related potentials (ERPs) were calculated for each cluster and condition. Next, a Generalized Partial Directed Coherence (gPDC) analysis was performed on each cluster to compare the functional connectivity between conditions and tasks.Main results. IC analysis of EEG during TSS resulted in three clusters identified at Brodmann areas (BA) 9, BA 6, and BA 4, which are areas associated with working memory, planning, and movement control. Lastly, we found significant (p < 0.05, adjusted for multiple comparisons) increases and decreases in functional connectivity of clusters during TSS, but not during FES when compared to the no stimulation conditions.Significance.The findings from this study provide evidence of how TSS recruits cortical networks during tonic and rhythmic lower limb movements. These results have implications for the development of spinal cord-based computer interfaces, and the design of neural stimulation devices for the treatment of pain and sensorimotor deficit.

Characterization of interlimb interaction via transcutaneous spinal stimulation of cervical and lumbar spinal enlargements.

The use of transcutaneous electrical spinal stimulation (TSS) to modulate sensorimotor networks after neurological insult has garnered much attention from both researchers and clinicians in recent years. Although many different stimulation paradigms have been reported, the interlimb effects of these neuromodulation techniques have been little studied. The effects of multisite TSS on interlimb sensorimotor function are of particular interest in the context of neurorehabilitation, as these networks have been shown to be important for functional recovery after neurological insult. The present study utilized a condition-test paradigm to investigate the effects of interenlargement TSS on spinal motor excitability in both cervical and lumbosacral motor pools. Additionally, comparison was made between the conditioning effects of lumbosacral and cervical TSS and peripheral stimulation of the fibular nerve and ulnar nerve, respectively. In 16/16 supine, relaxed participants, facilitation of spinally evoked motor responses (sEMRs) in arm muscles was seen in response to lumbosacral TSS or fibular nerve stimulation, whereas facilitation of sEMRs in leg muscles was seen in response to cervical TSS or ulnar nerve stimulation. The decreased latency between TSS- and peripheral nerve-evoked conditioning implicates interlimb networks in the observed facilitation of motor output. The results demonstrate the ability of multisite TSS to engage interlimb networks, resulting in the bidirectional influence of cervical and lumbosacral motor output. The engagement of interlimb networks via TSS of the cervical and lumbosacral enlargements represents a feasible method for engaging spinal sensorimotor networks in clinical populations with compromised motor function.NEW & NOTEWORTHY Bidirectional interlimb modulation of spinal motor excitability can be evoked by transcutaneous spinal stimulation over the cervical and lumbosacral enlargements. Multisite transcutaneous spinal stimulation engages spinal sensorimotor networks thought to be important in the recovery of function after spinal cord injury.

Detecting Endpoint Error of an Ongoing Reaching Movement: the Role of Vision, Proprioception, and Efference.

Brief windows of vision presented during reaching movements contribute to endpoint error estimates. It is not clear whether such error detection processes depend on other sources of information (e.g., proprioception and efference). In the current study, participants were presented with a brief window of vision and then judged whether their movement endpoint under- or over-shot the target after: 1) performing an active reach; 2) being passively guided by a robotic arm; and 3) observing a fake hand moved by the robot arm. Participants were most accurate at estimating their endpoint error in the active movement conditions and least accurate in the action observation condition. Thus, both efferent and proprioceptive information significantly contribute to endpoint error detection processes even with brief visual feedback.

Transcutaneous spinal cord stimulation improves postural stability in individuals with multiple sclerosis.

BACKGROUND: Widespread demyelination in the central nervous system can lead to progressive sensorimotor impairments following multiple sclerosis, with compromised postural stability during standing being a common consequence. As such, clinical strategies are needed to improve postural stability following multiple sclerosis. The objective of this study was therefore to investigate the effect of non-invasive transcutaneous spinal stimulation on postural stability during upright standing in individuals with multiple sclerosis. METHODS: Center of pressure displacement and electromyograms from the soleus and tibialis anterior were recorded in seven individuals with multiple sclerosis during standing without and with transcutaneous spinal stimulation. Center of pressure and muscle activity measures were calculated and compared between no stimulation and transcutaneous spinal stimulation conditions. The relationship between the center of pressure displacement and electromyograms was quantified using cross-correlation analysis. RESULTS: For transcutaneous spinal stimulation, postural stability was significantly improved during standing with eyes closed: the time- and frequency-domain measures obtained from the anterior-posterior center of pressure fluctuation decreased and increased, respectively, and the tibialis anterior activity was lower compared to no stimulation. Conversely, no differences were found between no stimulation and transcutaneous spinal stimulation when standing with eyes open. CONCLUSION: Following multiple sclerosis, transcutaneous spinal stimulation improved postural stability during standing with eyes closed, presumably by catalyzing proprioceptive function. Future work should confirm underlying mechanisms and explore the clinical value of transcutaneous spinal stimulation for individuals with multiple sclerosis.

The relationship between maximum tolerance and motor activation during transcutaneous spinal stimulation is unaffected by the carrier frequency or vibration.

Transcutaneous spinal stimulation (TSS) is a useful tool to modulate spinal sensorimotor circuits and has emerged as a potential treatment for motor disorders in neurologically impaired populations. One major limitation of TSS is the discomfort associated with high levels of stimulation during the experimental procedure. The objective of this study was to examine if the discomfort caused by TSS can be alleviated using different stimulation paradigms in a neurologically intact population. Tolerance to TSS delivered using conventional biphasic balanced rectangular pulses was compared to two alternative stimulation paradigms: a 5 kHz carrier frequency and biphasic balanced rectangular pulses combined with vibrotactile stimulation. In ten healthy participants, tolerance to TSS was examined using both single-pulse (0.2 Hz) and continuous (30 Hz) stimulation protocols. In both the single-pulse and continuous stimulation protocols, participants tolerated significantly higher levels of stimulation with the carrier frequency paradigm compared to the other stimulation paradigms. However, when the maximum tolerable stimulation intensity of each stimulation paradigm was normalized to the intensity required to evoke a lower limb muscle response, there were no statistical differences between the stimulation paradigms. Our results suggest that, when considering the intensity of stimulation required to obtain spinally evoked motor potentials, neither alternative stimulation paradigm is more effective at reducing discomfort than the conventional, unmodulated pulse configuration.

Age-related Differences in Sensorimotor Transformations for Visual and/or Somatosensory Targets: Planning or Execution?

Background: Older and younger adults utilize sensory information differently to plan and control their reaching movements to visual targets. In addition, younger adults appear to utilize different sensorimotor transformations when reaching to somatosensory vs. visual targets. Critically, it is not yet known if older adults perform similar sensorimotor transformations when planning and executing movements to targets of varying modalities (i.e., visual, somatosensory or bimodal).Methods: Participants (12 younger adults, mean age: 22; 12 older adults, mean age: 67) performed reaches with their right upper-limb to visual, somatosensory, and bimodal (i.e., visual-somatosensory) targets in a dark room. Data were ultimately analyzed using a 2 Age-Group by 3-Target Modality ANOVA.Results: For both age groups, endpoint precision was best when the visual target was presented (i.e., visual or bimodal). Critically, older adults exhibited longer reaction time (RT) compared to younger adults, especially when initiating reaches to the somatosensory targets (Cohen's d = 0.95). These longer RT's for older adults when aiming to somatosensory targets may indicate that aging leads to deficits in performing the sensorimotor transformations necessary to plan a reaching movement toward somatosensory targets. In contrast, control mechanisms during reaching execution appear to be comparable for both younger and older adults.Conclusions: When performing a voluntary movement to a felt vs. a seen target location, older adults appear to have altered planning mechanisms, compared to younger adults. Specifically, they tend to take more time to complete the necessary sensorimotor transformations to locate a somatosensory target. These findings could be used to guide the design of physical activity and rehabilitation protocols.

Two Neural Circuits to Point Towards Home Position After Passive Body Displacements.

A challenge in motor control research is to understand the mechanisms underlying the transformation of sensory information into arm motor commands. Here, we investigated these transformation mechanisms for movements whose targets were defined by information issued from body rotations in the dark (i.e., idiothetic information). Immediately after being rotated, participants reproduced the amplitude of their perceived rotation using their arm (Experiment 1). The cortical activation during movement planning was analyzed using electroencephalography and source analyses. Task-related activities were found in regions of interest (ROIs) located in the prefrontal cortex (PFC), dorsal premotor cortex, dorsal region of the anterior cingulate cortex (ACC) and the sensorimotor cortex. Importantly, critical regions for the cognitive encoding of space did not show significant task-related activities. These results suggest that arm movements were planned using a sensorimotor-type of spatial representation. However, when a 8 s delay was introduced between body rotation and the arm movement (Experiment 2), we found that areas involved in the cognitive encoding of space [e.g., ventral premotor cortex (vPM), rostral ACC, inferior and superior posterior parietal cortex (PPC)] showed task-related activities. Overall, our results suggest that the use of a cognitive-type of representation for planning arm movement after body motion is necessary when relevant spatial information must be stored before triggering the movement.

Preferential activation of spinal sensorimotor networks via lateralized transcutaneous spinal stimulation in neurologically intact humans.

Transcutaneous spinal stimulation (TSS), a noninvasive technique to modulate sensorimotor circuitry within the spinal cord, has been shown to enable a wide range of functions that were thought to be permanently impaired in humans with spinal cord injury. However, the extent to which TSS can be used to target specific mediolateral spinal cord circuitry remains undefined. We tested the hypothesis that TSS applied unilaterally to the skin ~2 cm lateral to the midline of the lumbosacral spine selectively activates ipsilateral spinal sensorimotor circuitry, resulting in ipsilateral activation of downstream lower extremity neuromusculature. TSS cathodes and anodes were positioned lateral from the midline of the spine in 15 healthy subjects while supine, and the timing of TSS pulses was synchronized to recordings of lower extremity muscle activity and force. At motor threshold, left and right TSS-evoked muscle activity was significantly higher in the ipsilateral leg compared with contralateral recordings from the same muscles. Similarly, we observed a significant increase in force production in the ipsilateral leg compared with the contralateral leg. Delivery of paired TSS pulses, during which an initial stimulus was applied to one side of the spinal cord and 50 ms later a second stimulus was applied to the contralateral side, revealed that ipsilateral leg muscle responses decreased following the initial stimulus, whereas contralateral muscle responses did not decrease, indicating side-specific activation of lateral spinal sensorimotor circuitry. Our results indicate TSS can selectively engage ipsilateral neuromusculature via lumbosacral sensorimotor networks responsible for lower extremity function in healthy humans.NEW & NOTEWORTHY We demonstrate the selectivity of transcutaneous spinal stimulation (TSS), which has been shown to enable function in humans with chronic paralysis. Specifically, we demonstrate that TSS applied to locations lateral to the spinal cord can selectively activate ipsilateral spinal sensorimotor networks. We quantified lumbosacral spinal network activity by recording lower extremity muscle electromyography and force. Our results suggest lumbosacral TSS engages side-specific spinal sensorimotor networks associated with ipsilateral lower extremity function in humans.

Auditory cues for somatosensory targets invoke visuomotor transformations: Behavioral and electrophysiological evidence.

Prior to goal-directed actions, somatosensory target positions can be localized using either an exteroceptive or an interoceptive body representation. The goal of the present study was to investigate if the body representation selected to plan reaches to somatosensory targets is influenced by the sensory modality of the cue indicating the target's location. In the first experiment, participants reached to somatosensory targets prompted by either an auditory or a vibrotactile cue. As a baseline condition, participants also performed reaches to visual targets prompted by an auditory cue. Gaze-dependent reaching errors were measured to determine the contribution of the exteroceptive representation to motor planning processes. The results showed that reaches to both auditory-cued somatosensory targets and auditory-cued visual targets exhibited larger gaze-dependent reaching errors than reaches to vibrotactile-cued somatosensory targets. Thus, an exteroceptive body representation was likely used to plan reaches to auditory-cued somatosensory targets but not to vibrotactile-cued somatosensory targets. The second experiment examined the influence of using an exteroceptive body representation to plan movements to somatosensory targets on pre-movement neural activations. Cortical responses to a task-irrelevant visual flash were measured as participants planned movements to either auditory-cued somatosensory or auditory-cued visual targets. Larger responses (i.e., visual-evoked potentials) were found when participants planned movements to somatosensory vs. visual targets, and source analyses revealed that these activities were localized to the left occipital and left posterior parietal areas. These results suggest that visual and visuomotor processing networks were more engaged when using the exteroceptive body representation to plan movements to somatosensory targets, than when planning movements to external visual targets.

Rapid online corrections for upper limb reaches to perturbed somatosensory targets: evidence for non-visual sensorimotor transformation processes.

When performing upper limb reaches, the sensorimotor system can adjust to changes in target location even if the reaching limb is not visible. To accomplish this task, sensory information about the new target location and the current position of the unseen limb are used to program online corrections. Previous researchers have argued that, prior to the initiation of corrections, somatosensory information from the unseen limb must be transformed into a visual reference frame. However, most of these previous studies involved movements to visual targets. The purpose of the present study was to determine if visual sensorimotor transformations are also necessary for the online control of movements to somatosensory targets. Participants performed reaches towards somatosensory and visual targets without vision of their reaching limb. Target positions were either stationary, or perturbed before (~ 450 ms), or after movement onset (~ 100 ms or ~ 200 ms). In response to target perturbations after movement onset, participants exhibited shorter correction latencies, larger correction magnitudes, and smaller movement endpoint errors when they reached to somatosensory targets as compared to visual targets. Because reference frame transformations have been shown to increase both processing time and errors, these results indicate that hand position was not transformed into visual reference frame during online corrections for movements to somatosensory targets. These findings support the idea that different sensorimotor transformations are used for the online control of movements to somatosensory and visual targets.

Action possibility judgments of people with varying motor abilities due to spinal cord injury.

Predictions about one's own action capabilities as well as the action capabilities of others are thought to be based on a simulation process involving linked perceptual and motor networks. Given the central role of motor experience in the formation of these networks, one's present motor capabilities are thought to be the basis of their perceptual judgments about actions. However, it remains unknown whether the ability to form these action possibility judgments is affected by performance related changes in the motor system. To determine if judgments of action capabilities are affected by long-term changes in one's own motor capabilities, participants with different degrees of upper-limb function due to their level (cervical vs. below cervical) of spinal cord injury (SCI) were tested on a perceptual-motor judgment task. Participants observed apparent motion videos of reciprocal aiming movements with varying levels of difficulty. For each movement, participants determined the shortest movement time (MT) at which they themselves and a young adult could perform the task while maintaining accuracy. Participants also performed the task. Analyses of MTs revealed that perceptual judgments for participant's own movement capabilities were consistent with their actual performance- people with cervical SCI had longer judged and actual MTs than people with below cervical SCI. However, there were no between-group differences in judged MTs for the young adult. Although it is unclear how the judgments were adjusted (altered simulation vs. threshold modification), the data reveal that people with different motor capabilities due to SCI are not completely biased by their present capabilities and can effectively adjust their judgments to estimate the actions of others.

Effects of robotic guidance on sensorimotor control: planning vs. online control?

BACKGROUND: Robotic guidance has been shown to facilitate motor skill acquisition, through altered sensorimotor control, in neurologically impaired and healthy populations. OBJECTIVE: To determine if robot-guided practice and online visual feedback availability primarily influences movement planning or online control mechanisms. METHODS: In this two-experiment study, participants first performed a pre-test involving reaches with or without vision, to obtain baseline measures. In both experiments, participants then underwent an acquisition phase where they either actively followed robot-guided trajectories or trained unassisted. Only in the second experiment, robot-guided or unassisted acquisition was performed either with or without online vision. Following acquisition, all participants completed a post-test that was the same as the pre-test. Planning and online control mechanisms were assessed through endpoint error and kinematic analyses. RESULTS: The robot-guided and unassisted groups generally exhibited comparable changes in endpoint accuracy and precision. Kinematic analyses revealed that only participants who practiced with the robot exhibited significantly reduced the proportion of movement time spent during the limb deceleration phase (i.e., time after peak velocity). This was true regardless of online visual feedback availability during training. CONCLUSION: The influence of robot-assisted motor skill acquisition is best explained by improved motor planning processes.

On the relationship between the execution, perception, and imagination of action.

Humans can perform, perceive, and imagine voluntary movement. Numerous investigations of these abilities have employed variants of goal-directed aiming tasks because the Fitts's law equation reliably captures the mathematical relationship between movement time (MT) and accuracy requirements. The emergence of Fitts's speed-accuracy relationship during movement execution, perception, and imagination has led to the suggestion that these processes rely on common neural codes. This common coding account is based on the notion that the neural codes used to generate an action are tightly bound to the codes that represent the perceptual consequences of that action. It is suggested that during action imagination and perception the bound codes are activated offline through an action simulation. The present study provided a comprehensive testing of this common coding hypothesis by examining the characteristics of the Fitts relationship in movement execution, perception, and imagination within the same individuals. Participants were required to imagine and perceive reciprocal aiming movements with varying accuracy requirements before and after actually executing the movements. Consistent with the common coding account, the Fitts relationship was observed in all conditions. Critically, the slopes of the regression lines across tasks were not different suggesting that the core of the speed-accuracy trade-off was consistent across conditions. In addition, it was found that incidental limb position variability scaled to the amplitude of imagined movements. This motor overflow suggests motor system activation during action imagination. Overall, the results support the hypothesis that action execution, perception, and imagination rely on a common coding system.

Facilitating the use of online visual feedback: advance information and the inter-trial interval?

Cheng et al. (2008) showed that when goal-directed reaching movements are performed with a 2.5 s inter-trial interval (ITI) under a randomized visual feedback schedule, individuals use online visual information on trial n to perform efficient online corrections on trial n + 1 (i.e., "reminiscence" effect). These results persisted even when participants were given knowledge of the up-coming vision condition. In this study, the ITI was extended to 5 s in an attempt to negate any effects of the preceding trial. Results from this study revealed that trials with vision were always more accurate than trials performed without vision, suggesting that individuals relied significantly on online information. Furthermore, aiming precision improved when participants knew the vision condition before each trial. It is thus suggested that the reminiscence effects are not longer evident with a 5 s ITI, which in turn allows prior knowledge of visual feedback to influence the use of online vision.