Brain Activation During Visually Guided Finger Movements.

Computer interaction via visually guided hand movements often employs either abstract cursor-based feedback or virtual hand (VH) representations of varying degrees of realism. The effect of changing this visual feedback in virtual reality settings is currently unknown. In this study, 19 healthy right-handed adults performed index finger movements ("action") and observed movements ("observation") with four different types of visual feedback: a simple circular cursor (CU), a point light (PL) pattern indicating finger joint positions, a shadow cartoon hand (SH) and a realistic VH. Finger movements were recorded using a data glove, and eye-tracking was recorded optically. We measured brain activity using functional magnetic resonance imaging (fMRI). Both action and observation conditions showed stronger fMRI signal responses in the occipitotemporal cortex compared to baseline. The action conditions additionally elicited elevated bilateral activations in motor, somatosensory, parietal, and cerebellar regions. For both conditions, feedback of a hand with a moving finger (SH, VH) led to higher activations than CU or PL feedback, specifically in early visual regions and the occipitotemporal cortex. Our results show the stronger recruitment of a network of cortical regions during visually guided finger movements with human hand feedback when compared to a visually incomplete hand and abstract feedback. This information could have implications for the design of visually guided tasks involving human body parts in both research and application or training-related paradigms.

Automated and Quantitative Assessment of Tactile Mislocalization After Stroke.

Topesthesia, the recognition of tactile stimulation location on the skin, can be severely affected by neurological injuries, such as stroke. Despite topesthesia being crucial for manipulating objects and interacting with the environment during activities of daily living, deficits cannot be quantitatively captured with current clinical assessments and are, as a consequence, not well-understood. The present work describes a novel automated assessment tool for tactile mislocalization in neurological patients with somatosensory deficits. We present two cases of ischemic stroke patients, describe their tactile localization deficits with the automated assessment, and compare the results to a standard manual clinical assessment. Using the automated assessment tool, it was possible to identify, locate, precisely quantify, and depict the patients' deficits in topesthesia. In comparison, the clinical assessment was not sensitive enough and some deficits would remain undetected due to ceiling effects. In addition, an MRI structural analysis of the lesion supported the existence of somatosensory deficits. This novel and quantitative assessment may not only help to raise awareness of the implications of deficits in topesthesia, but would also allow monitoring recovery throughout the rehabilitation process, informing treatment design, and objectively evaluating treatment efficacy.

BOLD signal in sensorimotor regions reveals differential encoding of passive forefinger velocity and displacement amplitude.

Peripheral encoding of movement kinematics has been well-characterized, but there is little understanding of the relationship between movement kinematics and associated brain activation. We hypothesized that kinematics of passive movement is differentially represented in the sensorimotor network, reflecting the well-studied afferent responses to movement. A robotic forefinger manipulandum was used to induce passive kinematic stimuli and monitor interaction force in 41 healthy participants during whole-brain functional magnetic resonance imaging (fMRI). Levels of forefinger displacement amplitude and velocity were presented in flexion and extension. Increases in velocity were linearly associated with activation in contralateral primary somatosensory cortex (S1), bilateral secondary somatosensory cortex (S2), primary motor cortex, and supplementary motor area. No difference in activation was found for direction of the finger movement. Unexpectedly, S1 and S2 activation decreased nonlinearly with increasing displacement amplitude. We conclude that while straightforward relations were found with velocity, the complex neural representation of displacement amplitude suggests a more nuanced relationship between peripheral responses to kinematic stimuli and sensorimotor network activity. Here we present a novel, systematic characterization of the whole-brain response to passive movement kinematics.

Neural correlates of visuomotor adjustments during scaling of human finger movements.

Visually guided finger movements include online feedback of current effector position to guide target approach. This visual feedback may be scaled or otherwise distorted by unpredictable perturbations. Although adjustments to visual feedback scaling have been studied before, the underlying brain activation differences between upscaling (visual feedback larger than real movement) and downscaling (feedback smaller than real movement) are currently unknown. Brain activation differences between upscaling and downscaling might be expected because within-trial adjustments during upscaling require corrective backwards accelerations, whereas correcting for downscaling requires forward accelerations. In this behavioural and fMRI study we investigated adjustments during up- and downscaling in a target-directed finger flexion-extension task with real-time visual feedback. We found that subjects made longer and more complete within-trial corrections for downscaling perturbations than for upscaling perturbations. The finger task activated primary motor (M1) and somatosensory (S1) areas, premotor and parietal regions, basal ganglia, and cerebellum. General scaling effects were seen in the right pre-supplementary motor area, dorsal anterior cingulate cortex, inferior parietal lobule, and dorsolateral prefrontal cortex. Stronger activations for down- than for upscaling were observed in M1, supplementary motor area (SMA), S1 and anterior cingulate cortex. We argue that these activation differences may reflect differing online correction for upscaling vs. downscaling during finger flexion-extension.

Correction: Virtual Hand Feedback Reduces Reaction Time in an Interactive Finger Reaching Task.

[This corrects the article DOI: 10.1371/journal.pone.0154807.].

Virtual Hand Feedback Reduces Reaction Time in an Interactive Finger Reaching Task.

Computer interaction via visually guided hand or finger movements is a ubiquitous part of daily computer usage in work or gaming. Surprisingly, however, little is known about the performance effects of using virtual limb representations versus simpler cursors. In this study 26 healthy right-handed adults performed cued index finger flexion-extension movements towards an on-screen target while wearing a data glove. They received each of four different types of real-time visual feedback: a simple circular cursor, a point light pattern indicating finger joint positions, a cartoon hand and a fully shaded virtual hand. We found that participants initiated the movements faster when receiving feedback in the form of a hand than when receiving circular cursor or point light feedback. This overall difference was robust for three out of four hand versus circle pairwise comparisons. The faster movement initiation for hand feedback was accompanied by a larger movement amplitude and a larger movement error. We suggest that the observed effect may be related to priming of hand information during action perception and execution affecting motor planning and execution. The results may have applications in the use of body representations in virtual reality applications.

Relationship between structural brainstem and brain plasticity and lower-limb training in spinal cord injury: a longitudinal pilot study.

Rehabilitative training has shown to improve significantly motor outcomes and functional walking capacity in patients with incomplete spinal cord injury (iSCI). However, whether performance improvements during rehabilitation relate to brain plasticity or whether it is based on functional adaptation of movement strategies remain uncertain. This study assessed training improvement-induced structural brain plasticity in chronic iSCI patients using longitudinal MRI. We used tensor-based morphometry (TBM) to analyze longitudinal brain volume changes associated with intensive virtual reality (VR)-augmented lower limb training in nine traumatic iSCI patients. The MRI data was acquired before and after a 4-week training period (16-20 training sessions). Before training, voxel-based morphometry (VBM) and voxel-based cortical thickness (VBCT) assessed baseline morphometric differences in nine iSCI patients compared to 14 healthy controls. The intense VR-augmented training of limb control improved significantly balance, walking speed, ambulation, and muscle strength in patients. Retention of clinical improvements was confirmed by the 3-4 months follow-up. In patients relative to controls, VBM revealed reductions of white matter volume within the brainstem and cerebellum and VBCT showed cortical thinning in the primary motor cortex. Over time, TBM revealed significant improvement-induced volume increases in the left middle temporal and occipital gyrus, left temporal pole and fusiform gyrus, both hippocampi, cerebellum, corpus callosum, and brainstem in iSCI patients. This study demonstrates structural plasticity at the cortical and brainstem level as a consequence of VR-augmented training in iSCI patients. These structural changes may serve as neuroimaging biomarkers of VR-augmented lower limb neurorehabilitation in addition to performance measures to detect improvements in rehabilitative training.

Improvement in precision grip force control with self-modulation of primary motor cortex during motor imagery.

Motor imagery (MI) has shown effectiveness in enhancing motor performance. This may be due to the common neural mechanisms underlying MI and motor execution (ME). The main region of the ME network, the primary motor cortex (M1), has been consistently linked to motor performance. However, the activation of M1 during motor imagery is controversial, which may account for inconsistent rehabilitation therapy outcomes using MI. Here, we examined the relationship between contralateral M1 (cM1) activation during MI and changes in sensorimotor performance. To aid cM1 activity modulation during MI, we used real-time fMRI neurofeedback-guided MI based on cM1 hand area blood oxygen level dependent (BOLD) signal in healthy subjects, performing kinesthetic MI of pinching. We used multiple regression analysis to examine the correlation between cM1 BOLD signal and changes in motor performance during an isometric pinching task of those subjects who were able to activate cM1 during motor imagery. Activities in premotor and parietal regions were used as covariates. We found that cM1 activity was positively correlated to improvements in accuracy as well as overall performance improvements, whereas other regions in the sensorimotor network were not. The association between cM1 activation during MI with performance changes indicates that subjects with stronger cM1 activation during MI may benefit more from MI training, with implications toward targeted neurotherapy.

Suppression of enhanced physiological tremor via stochastic noise: initial observations.

Enhanced physiological tremor is a disabling condition that arises because of unstable interactions between central tremor generators and the biomechanics of the spinal stretch reflex. Previous work has shown that peripheral input may push the tremor-related spinal and cortical systems closer to anti-phase firing, potentially leading to a reduction in tremor through phase cancellation. The aim of the present study was to investigate whether peripherally applied mechanical stochastic noise can attenuate enhanced physiological tremor and improve motor performance. Eight subjects with enhanced physiological tremor performed a visuomotor task requiring the right index finger to compensate a static force generated by a manipulandum to which Gaussian noise (3-35 Hz) was applied. The finger position was displayed on-line on a monitor as a small white dot which the subjects had to maintain in the center of a larger green circle. Electromyogram (EMG) from the active hand muscles and finger position were recorded. Performance was measured by the mean absolute deviation of the white dot from the zero position. Tremor was identified by the acceleration in the frequency range 7-12 Hz. Two different conditions were compared: with and without superimposed noise at optimal amplitude (determined at the beginning of the experiment). The application of optimum noise reduced tremor (accelerometric amplitude and EMG activity) and improved the motor performance (reduced mean absolute deviation from zero). These data provide the first evidence of a significant reduction of enhanced physiological tremor in the human sensorimotor system due to application of external stochastic noise.

Enhanced corticomuscular coherence by external stochastic noise.

Noise can have beneficial effects as shown by the stochastic resonance (SR) phenomenon which is characterized by performance improvement when an optimal noise is added. Modern attempts to improve human performance utilize this phenomenon. The purpose of the present study was to investigate whether performance improvement by addition of optimum noise (ON) is related to increased cortical motor spectral power (SP) and increased corticomuscular coherence. Eight subjects performed a visuomotor task requiring to compensate with the right index finger a static force (SF) generated by a manipulandum on which Gaussian noise was applied. The finger position was displayed on-line on a monitor as a small white dot which the subjects had to maintain in the center of a green bigger circle. Electroencephalogram from the contralateral motor area, electromyogram from active muscles and finger position were recorded. The performance was measured by the mean absolute deviation (MAD) of the white dot from the zero position. ON compared to the zero noise condition induced an improvement in motor accuracy together with an enhancement of cortical motor SP and corticomuscular coherence in beta-range. These data suggest that the improved sensorimotor performance via SR is consistent with an increase in the cortical motor SP and in the corticomuscular coherence.

A reliability study on brain activation during active and passive arm movements supported by an MRI-compatible robot.

In neurorehabilitation, longitudinal assessment of arm movement related brain function in patients with motor disability is challenging due to variability in task performance. MRI-compatible robots monitor and control task performance, yielding more reliable evaluation of brain function over time. The main goals of the present study were first to define the brain network activated while performing active and passive elbow movements with an MRI-compatible arm robot (MaRIA) in healthy subjects, and second to test the reproducibility of this activation over time. For the fMRI analysis two models were compared. In model 1 movement onset and duration were included, whereas in model 2 force and range of motion were added to the analysis. Reliability of brain activation was tested with several statistical approaches applied on individual and group activation maps and on summary statistics. The activated network included mainly the primary motor cortex, primary and secondary somatosensory cortex, superior and inferior parietal cortex, medial and lateral premotor regions, and subcortical structures. Reliability analyses revealed robust activation for active movements with both fMRI models and all the statistical methods used. Imposed passive movements also elicited mainly robust brain activation for individual and group activation maps, and reliability was improved by including additional force and range of motion using model 2. These findings demonstrate that the use of robotic devices, such as MaRIA, can be useful to reliably assess arm movement related brain activation in longitudinal studies and may contribute in studies evaluating therapies and brain plasticity following injury in the nervous system.

Broad-band Gaussian noise is most effective in improving motor performance and is most pleasant.

Modern attempts to improve human performance focus on stochastic resonance (SR). SR is a phenomenon in non-linear systems characterized by a response increase of the system induced by a particular level of input noise. Recently, we reported that an optimum level of 0-15 Hz Gaussian noise applied to the human index finger improved static isometric force compensation. A possible explanation was a better sensorimotor integration caused by increase in sensitivity of peripheral receptors and/or of internal SR. The present study in 10 subjects compares SR effects in the performance of the same motor task and on pleasantness, by applying three Gaussian noises chosen on the sensitivity of the fingertip receptors (0-15 Hz mostly for Merkel receptors, 250-300 Hz for Pacini corpuscles and 0-300 Hz for all). We document that only the 0-300 Hz noise induced SR effect during the transitory phase of the task. In contrast, the motor performance was improved during the stationary phase for all three noise frequency bandwidths. This improvement was stronger for 0-300 Hz and 250-300 Hz than for 0-15 Hz noise. Further, we found higher degree of pleasantness for 0-300 Hz and 250-300 Hz noise bandwidths than for 0-15 Hz. Thus, we show that the most appropriate Gaussian noise that could be used in haptic gloves is the 0-300 Hz, as it improved motor performance during both stationary and transitory phases. In addition, this noise had the highest degree of pleasantness and thus reveals that the glabrous skin can also forward pleasant sensations.

Delineating the whole brain BOLD response to passive movement kinematics.

The field of brain-machine interfaces (BMIs) has made great advances in recent years, converting thought to movement, with some of the most successful implementations measuring directly from the motor cortex. However, the ability to record from additional regions of the brain could potentially improve flexibility and robustness of use. In addition, BMIs of the future will benefit from integrating kinesthesia into the control loop. Here, we examine whether changes in passively induced forefinger movement amplitude are represented in different regions than forefinger velocity via a MR compatible robotic manipulandum. Using functional magnetic resonance imaging (fMRI), five healthy participants were exposed to combinations of forefinger movement amplitude and velocity in a factorial design followed by an epoch-based analysis. We found that primary and secondary somatosensory regions were activated, as well as cingulate motor area, putamen and cerebellum, with greater activity from changes in velocity compared to changes in amplitude. This represents the first investigation into whole brain response to parametric changes in passive movement kinematics. In addition to informing BMIs, these results have implications towards neural correlates of robotic rehabilitation.

Enhanced activation of motor execution networks using action observation combined with imagination of lower limb movements.

The combination of first-person observation and motor imagery, i.e. first-person observation of limbs with online motor imagination, is commonly used in interactive 3D computer gaming and in some movie scenes. These scenarios are designed to induce a cognitive process in which a subject imagines himself/herself acting as the agent in the displayed movement situation. Despite the ubiquity of this type of interaction and its therapeutic potential, its relationship to passive observation and imitation during observation has not been directly studied using an interactive paradigm. In the present study we show activation resulting from observation, coupled with online imagination and with online imitation of a goal-directed lower limb movement using functional MRI (fMRI) in a mixed block/event-related design. Healthy volunteers viewed a video (first-person perspective) of a foot kicking a ball. They were instructed to observe-only the action (O), observe and simultaneously imagine performing the action (O-MI), or imitate the action (O-IMIT). We found that when O-MI was compared to O, activation was enhanced in the ventralpremotor cortex bilaterally, left inferior parietal lobule and left insula. The O-MI and O-IMIT conditions shared many activation foci in motor relevant areas as confirmed by conjunction analysis. These results show that (i) combining observation with motor imagery (O-MI) enhances activation compared to observation-only (O) in the relevant foot motor network and in regions responsible for attention, for control of goal-directed movements and for the awareness of causing an action, and (ii) it is possible to extensively activate the motor execution network using O-MI, even in the absence of overt movement. Our results may have implications for the development of novel virtual reality interactions for neurorehabilitation interventions and other applications involving training of motor tasks.

Virtual reality-augmented neurorehabilitation improves motor function and reduces neuropathic pain in patients with incomplete spinal cord injury.

BACKGROUND: Neurorehabilitation interventions to improve lower limb function and neuropathic pain have had limited success in people with chronic, incomplete spinal cord injury (iSCI). OBJECTIVE: We hypothesized that intense virtual reality (VR)-augmented training of observed and executed leg movements would improve limb function and neuropathic pain. METHODS: Patients used a VR system with a first-person view of virtual lower limbs, controlled via movement sensors fitted to the patient's own shoes. Four tasks were used to deliver intensive training of individual muscles (tibialis anterior, quadriceps, leg ad-/abductors). The tasks engaged motivation through feedback of task success. Fourteen chronic iSCI patients were treated over 4 weeks in 16 to 20 sessions of 45 minutes. Outcome measures were 10 Meter Walking Test, Berg Balance Scale, Lower Extremity Motor Score, Spinal Cord Independence Measure, Locomotion and Neuropathic Pain Scale (NPS), obtained at the start and at 4 to 6 weeks before intervention. RESULTS: In addition to positive changes reported by the patients (Patients' Global Impression of Change), measures of walking capacity, balance, and strength revealed improvements in lower limb function. Intensity and unpleasantness of neuropathic pain in half of the affected participants were reduced on the NPS test. Overall findings remained stable 12 to 16 weeks after termination of the training. CONCLUSIONS: In a pretest/posttest, uncontrolled design, VR-augmented training was associated with improvements in motor function and neuropathic pain in persons with chronic iSCI, several of which reached the level of a minimal clinically important change. A controlled trial is needed to compare this intervention to active training alone or in combination.

The strength of the corticospinal coherence depends on the predictability of modulated isometric forces.

Isometric compensation of predictably frequency-modulated low forces is associated with corticomuscular coherence (CMC) in beta and low gamma range. It remains unclear how the CMC is influenced by unpredictably modulated forces, which create a mismatch between expected and actual sensory feedback. We recorded electroencephalography from the contralateral hand motor area, electromyography (EMG), and the motor performance of 16 subjects during a visuomotor task in which they had to isometrically compensate target forces at 8% of the maximum voluntary contraction with their right index finger. The modulated forces were presented with predictable or unpredictable frequencies. We calculated the CMC, the cortical motor alpha-, beta-, and gamma-range spectral powers (SP), and the task-related desynchronization (TRD), as well as the EMG SP and the performance. We found that in the unpredictable condition the CMC was significantly lower and associated with lower cortical motor SP, stronger TRD, higher EMG SP, and worse performance. The findings suggest that due to the mismatch between predicted and actual sensory feedback leading to higher computational load and less stationary motor state, the unpredictable modulation of the force leads to a decrease in corticospinal synchrony, an increase in cortical and muscle activation, and a worse performance.

Improved sensorimotor performance via stochastic resonance.

Several studies about noise-enhanced balance control in humans support the hypothesis that stochastic resonance can enhance the detection and transmission in sensorimotor system during a motor task. The purpose of the present study was to extend these findings in a simpler and controlled task. We explored whether a particular level of a mechanical Gaussian noise (0-15 Hz) applied on the index finger can improve the performance during compensation for a static force generated by a manipulandum. The finger position was displayed on a monitor as a small white point in the center of a gray circle. We considered a good performance when the subjects exhibited a low deviation from the center of this circle and when the performance had less variation over time. Several levels of mechanical noise were applied on the manipulandum. We compared the performance between zero noise (ZN), optimal noise (ON), and high noise (HN). In all subjects (8 of 8) the data disclosed an inverted U-like graph between the inverse of the mean variation in position and the input noise level. In other words, the mean variation was significantly smaller during ON than during ZN or HN. The findings suggest that the application of a tactile-proprioceptive noise can improve the stability in sensorimotor performance via stochastic resonance. Possible explanations for this improvement in motor precision are an increase of the peripheral receptors sensitivity and of the internal stochastic resonance, causing a better sensorimotor integration and an increase in corticomuscular synchronization.

Impact of a weekly dance class on the functional mobility and on the quality of life of individuals with Parkinson's disease.

Individuals with Parkinson's disease (PD) mainly suffer from motor impairments which increase the risk of falls and lead to a decline of quality of life. Several studies investigated the long-term effect of dance for people with PD. The aims of the present study were to investigate (i) the short-term effects of dance (i.e., the effect immediately after the dance class) on motor control in individuals with PD and (ii) the long-term effects of 8 months of participation in the weekly dance class on the quality of life of the PD patients and their caregivers. The dance lessons took place in a ballet studio and were led by a professional dancer. Eleven people with moderate to severe PD (58-85 years old) were subjected to a motor and quality of life assessments. With respect to the motor assessments the unified Parkinson disease rating scale III (UPDRS III), the timed up and go test (TUG), and the Semitandem test (SeTa) before and after the dance class were used. With respect to the quality of life and well-being we applied quality of life scale (QOLS) as well as the Westheimer questionnaire. Additionally, we asked the caregivers to fill out the Questionnaire for caregivers. We found a significant beneficial short-term effect for the total score of the UPDRS motor score. The strongest improvements were in rigidity scores followed by significant improvements in hand movements, finger taps, and facial expression. No significant changes were found for TUG and for SeTa. The results of the questionnaires showed positive effects of the dance class on social life, health, body-feeling and mobility, and on everyday life competences of the PD patients. Beneficial effect was also found for the caregivers. The findings demonstrate that dance has beneficial effect on the functional mobility of individuals with PD. Further, dance improves the quality of life of the patients and their caregivers. Dance may lead to better therapeutic strategies as it is engaging and enjoyable.

Movement observation activates lower limb motor networks in chronic complete paraplegia.

BACKGROUND: In healthy subjects, observation of actions activates a motor network similar to that involved in the performance of the observed actions. Movement observation could perhaps be applied to functionally sustain brain motor functions when efferent motor commands and proprioceptive feedbacks are disconnected. OBJECTIVE: The authors examined whether observation-induced brain activation is preserved in people with chronic complete spinal cord injury (SCI). METHODS: Nine patients and 12 healthy subjects underwent behavioral assessment and functional magnetic resonance imaging. The SCI patients attempted to perform dorsal and plantar flexions of the right foot, and the controls also executed the same movement. Both groups observed subsequent video clips showing the same movement. RESULTS: In the SCI group, attempted and observed foot movements activated a common observation-execution network including ventral premotor, parietal cortex, and cerebellum as in healthy subjects. CONCLUSIONS: Long after onset of complete SCI, the brain maintains its ability to respond to task-specific visual inputs, which suggests preservation of motor programs. This persistence might be a prerequisite for repair strategies of the spinal cord that rely on appropriate activation of the brain to try to restore limb function. The preserved cortical network may offer an additional motor rehabilitation approach for people with SCI.

fMRI assessment of upper extremity related brain activation with an MRI-compatible manipulandum.

PURPOSE: Longitudinal studies to evaluate the effect of rehabilitative therapies require an objective, reproducible and quantitative means for testing function in vivo. An fMRI assessment tool for upper extremity related brain activation using an MRI-compatible manipulandum was developed and tested for use in neurorehabilitation research. METHODS: Fifteen healthy, right-handed subjects participated in two fMRI sessions, which were three to four weeks apart. A block design paradigm, composed of three conditions of subject-passive movement, subject-active movement and rest, was employed for the fMRI recordings. During the rest condition, subjects simply held the device handle without applying any force or movement. The same type of auditory and visual instructions were given in all the three conditions, guiding the subjects to perform the motor tasks interactively with the MRI-compatible arm manipulandum. The tasks were controlled across the fMRI sessions. The subjects' brain activation was recorded by fMRI, and their behavioral performance was recorded by the manipulandum. The brain network activated by the subjects' interaction with the manipulandum was identified, and the reproducibility and reliability of the obtained activation were determined. RESULTS: All subjects completed the trial protocol. Two subjects were excluded from analysis due to head motion artifacts. All passive movements were performed well. Four out of the total 780 active movements were missed by two subjects. Brain activation was found in the contralateral sensorimotor cortex, secondary somatosensory cortex and non-primary motor cortex as well as in subcortical areas in the thalamus, basal ganglia and the cerebellum. These activations were consistent across the two fMRI sessions. CONCLUSION: The MRI-compatible manipulandum elicited robust and reproducible brain activations in healthy subjects during the subject-active and subject-passive upper extremity motor tasks with a block design paradigm. This system is promising for many applications in neurorehabilitation research and may be useful for longitudinal studies.