Alpha-band activity in parietofrontal cortex predicts future availability of vibrotactile feedback in prosthesis use.

Prosthesis disuse and abandonment is an ongoing issue in upper-limb amputation. In addition to lost structural and motor function, amputation also results in decreased task-specific sensory information. One proposed remedy is augmenting somatosensory information using vibrotactile feedback to provide tactile feedback of grasping objects. While the role of frontal and parietal areas in motor tasks is well established, the neural and kinematic effects of this augmented vibrotactile feedback remain in question. In this study, we sought to understand the neurobehavioral effects of providing augmented feedback during a reach-grasp-transport task. Ten persons with sound limbs performed a motor task while wearing a prosthesis simulator with and without vibrotactile feedback. We hypothesized that providing vibrotactile feedback during prosthesis use would increase activity in frontal and parietal areas and improve grasp-related behavior. Results show that anticipation of upcoming vibrotactile feedback may be encoded in motor and parietal areas during the reach-to-grasp phase of the task. While grasp aperture is unaffected by vibrotactile feedback, the availability of vibrotactile feedback does lead to a reduction in velocity during object transport. These results help shed light on how engineered feedback is utilized by prostheses users and provide methodologies for further assessment in advanced prosthetics research.

Flexible constraint hierarchy during the visual encoding of tool-object interactions.

Tools and objects are associated with numerous action possibilities that are reduced depending on the task-related internal and external constraints presented to the observer. Action hierarchies propose that goals represent higher levels of the hierarchy while kinematic patterns represent lower levels of the hierarchy. Prior work suggests that tool-object perception is heavily influenced by grasp and action context. The current study sought to evaluate whether the presence of action hierarchy can be perceptually identified using eye tracking during tool-object observation. We hypothesize that gaze patterns will reveal a perceptual hierarchy based on the observed task context and grasp constraints. Participants viewed tool-objects scenes with two types of constraints: task-context and grasp constraints. Task-context constraints consisted of correct (e.g., frying pan-spatula) and incorrect tool-object pairings (e.g., stapler-spatula). Grasp constraints involved modified tool orientations, which requires participants to understand how initially awkward grasp postures can help achieve the task. The visual scene contained three areas of interests (AOIs): the object, the functional tool-end (e.g., spoon handle) and the manipulative tool-end (e.g., spoon bowl). Results revealed two distinct processes based on stimuli constraints. Goal-oriented encoding, the attentional bias towards the object and manipulative tool-end, was demonstrated when grasp did not lead to meaningful tool-use. In images where grasp postures were critical to action performance, attentional bias was primarily between the object and functional tool-end, which suggests means-related encoding of the graspable properties of the object. This study expands from previous work and demonstrates a flexible constraint hierarchy depending on the observed task constraints.

Neurorehabilitation in upper limb amputation: understanding how neurophysiological changes can affect functional rehabilitation.

BACKGROUND: Significant advances have been made in developing new prosthetic technologies with the goal of restoring function to persons that suffer partial or complete loss of the upper limb. Despite these technological advances, many challenges remain in understanding barriers in patient adoption of technology, and what critical factors should be of focus in prosthetics development from a motor control perspective. This points to a potential opportunity to improve our understanding of amputation using neurophysiology and plasticity, and integrate this knowledge into the development of prosthetics technology in novel ways. Here, argument will be made to include a stronger focus on the neural and behavioral changes that result from amputation, and a better appreciation of the time-scale of changes which may significantly affect device adaptation, functional device utility, and motor learning implemented in rehabilitation environments. CONCLUSION: By strengthening our understanding of the neuroscience of amputation, we may improve the ability to couple neurorehabilitation with neuroengineering to support clinician needs in yielding improved outcomes in patients.

Reliability of Visual and Somatosensory Feedback in Skilled Movement: The Role of the Cerebellum.

The integration of vision and somatosensation is required to allow for accurate motor behavior. While both sensory systems contribute to an understanding of the state of the body through continuous updating and estimation, how the brain processes unreliable sensory information remains to be fully understood in the context of complex action. Using functional brain imaging, we sought to understand the role of the cerebellum in weighting visual and somatosensory feedback by selectively reducing the reliability of each sense individually during a tool use task. We broadly hypothesized upregulated activation of the sensorimotor and cerebellar areas during movement with reduced visual reliability, and upregulated activation of occipital brain areas during movement with reduced somatosensory reliability. As specifically compared to reduced somatosensory reliability, we expected greater activations of ipsilateral sensorimotor cerebellum for intact visual and somatosensory reliability. Further, we expected that ipsilateral posterior cognitive cerebellum would be affected with reduced visual reliability. We observed that reduced visual reliability results in a trend towards the relative consolidation of sensorimotor activation and an expansion of cerebellar activation. In contrast, reduced somatosensory reliability was characterized by the absence of cerebellar activations and a trend towards the increase of right frontal, left parietofrontal activation, and temporo-occipital areas. Our findings highlight the role of the cerebellum for specific aspects of skillful motor performance. This has relevance to understanding basic aspects of brain functions underlying sensorimotor integration, and provides a greater understanding of cerebellar function in tool use motor control.

Motor performance benefits of matched limb imitation in prosthesis users.

Our previous work demonstrated that the action encoding parietofrontal network, which is crucial in planning and executing motor tasks, is less active in prosthesis users who imitate movements of intact actors (mismatched limb) versus prosthesis users (matched limb). Such activation could have behavioral consequences in prosthesis users rehabilitating with intact therapists. The goal was to identify behavioral effects of matched versus mismatched limb action imitation in naïve users of prostheses. Intact subjects donned a specially adapted prosthetic device to simulate the wrist and forearm movement that transradial amputees experience. While electrogoniometry was recorded, non-amputated prosthesis users (NAPUs) observed and imitated demonstrations of a skillful motor task performed by either an intact actor or NAPU. We hypothesized that NAPUs would elicit less motion variability when performing matched versus mismatched imitation. Matched imitation resulted in a significant decrease in shoulder motion variability compared with mismatched imitation. The matched group also developed elbow motion patterns similar to the NAPU demonstrator, while the mismatched group attempted patterns similar to the intact demonstrator. This suggests a behavioral advantage to matched imitation when adapting to a prosthetic device, as it yielded more consistent movements and facilitated development of new motor patterns. Further, these results suggest that when prosthesis users are faced with the impossible task of imitating movements of an intact hand, they perform this action with greater variability and poorer technique. This work has implications on how prosthetic device operation is conveyed to persons with amputation as their clinical interactions often involve mismatched limb imitation.

Grasp Posture Variability Leads to Greater Ipsilateral Sensorimotor Beta Activation During Simulated Prosthesis Use.

Motor behaviour using upper-extremity prostheses of different levels is greatly variable, leading to challenges interpreting ideal rehabilitation strategies. Elucidating the underlying neural control mechanisms driving variability benefits our understanding of adaptation after limb loss. In this follow-up study, non-amputated participants completed simple and complex reach-to-grasp motor tasks using a body-powered transradial or partial-hand prosthesis simulator. We hypothesised that under complex task constraints, individuals employing variable grasp postures will show greater sensorimotor beta activation compared to individuals relying on uniform grasping, and activation will occur later in variable compared to uniform graspers. In the simple task, partial-hand variable and transradial users showed increased neural activation from the early to late phase of the reach, predominantly in the hemisphere ipsilateral to device use. In the complex task, only partial-hand variable graspers showed a significant increase in neural activation of the sensorimotor cortex from the early to the late phase of the reach. These results suggest that grasp variability may be a crucial component in the mechanism of neural adaptation to prosthesis use, and may be mediated by device level and task complexity, with implications for rehabilitation after amputation.

Ventral encoding of functional affordances: a neural pathway for identifying errors in action.

Functional tool usage is a critical aspect of our daily lives. Not only must we know which tools to use for a specific action goal, we must also know how to manipulate those tools in meaningful way to achieve the goal of the action. The purpose of this study was to identify the regions of the brain critical to supporting the process of understanding errors in tool manipulation. Using fMRI, neural activations were recorded while subjects were presented with images demonstrating typical action scenes (screwdriver used on a screw), but with the tool being manipulated either correctly (screwdriver held by handle) or incorrectly (screwdriver held by bit rather than handle). Activations in fMRI for identifying correct over incorrect tool manipulation were seen along the canonical parietofrontal action network, while activations for identifying incorrect over correct tool manipulation were primarily seen at superior temporal areas and insula. We expand our hypotheses about ventral brain networks identifying contextual error to further suggest mechanisms for understanding functional tool actions, which collectively we regard as functional affordances. This proposes a fundamental role for ventral brain areas in functional action understanding.

One hand, two objects: emergence of affordance in contexts.

Studies on affordances typically focus on single objects. We investigated whether affordances are modulated by the context, defined by the relation between two objects and a hand. Participants were presented with pictures displaying two manipulable objects linked by a functional (knife-butter), a spatial (knife-coffee mug), or by no relation. They responded by pressing a key whether the objects were related or not. To determine if observing other's actions and understanding their goals would facilitate judgments, a hand was: (a) displayed near the objects; (b) grasping an object to use it; (c) grasping an object to manipulate/move it; (d) no hand was displayed. RTs were faster when objects were functionally rather than spatially related. Manipulation postures were the slowest in the functional context and functional postures were inhibited in the spatial context, probably due to mismatch between the inferred goal and the context. The absence of this interaction with foot responses instead of hands in Experiment 2 suggests that effects are due to motor simulation rather than to associations between context and hand-postures.

Neurorehabilitation in Adults With Traumatic Upper Extremity Amputation: A Scoping Review.

BACKGROUND: Most of the current literature around amputation focuses on lower extremity amputation or engineering aspects of prosthetic devices. There is a need to more clearly understand neurobehavioral mechanisms related to upper extremity amputation and how such mechanisms might influence recovery and utilization of prostheses. OBJECTIVE: This scoping review aims to identify and summarize the current literature on adult traumatic upper limb amputation in regard to recovery and functional outcomes and how neuroplasticity might influence these findings. METHODS: We identified appropriate articles using Academic Search Complete EBSCO, OVID Medline, and Cochrane databases. The resulting articles were then exported, screened, and reviewed based on Preferred Reporting Items for Systematic Reviews and Meta-Analyses for Scoping Reviews (PRISMA-ScR) guidelines. RESULTS: Eleven (11) studies met the study criteria. Of these studies, 7 focused on sensory involvement, 3 focused on neuroplastic changes post-amputation related to functional impact, and 1 study focused on motor control and learning post-amputation. Overall, these studies revealed an incomplete understanding of the neural mechanisms involved in motor rehabilitation in the central and peripheral nervous systems, while also demonstrating the value of an individualized approach to neurorehabilitation in upper limb loss. CONCLUSIONS: There is a gap in our understanding of the role of neurorehabilitation following amputation. Overall, focused rehabilitation parameters, demographic information, and clarity around central and peripheral neural mechanisms are needed in future research to address neurobehavioral mechanisms to promote functional recovery following traumatic upper extremity amputation.

Partial-Hand Prosthesis Users Show Improved Reach-to-Grasp Behaviour Compared to Transradial Prosthesis Users with Increased Task Complexity.

Approaches to improve outcomes after upper-extremity amputation remain poorly understood. Examining prosthesis-use at different levels of loss elucidates motor control challenges. Non-amputated participants completed simple and complex reach-to-grasp actions using a body-powered transradial or partial-hand prosthesis simulator. We hypothesised that increased task complexity and participants using a partial-hand device would show greater functional adaptation compared to participants using a transradial device. Partial-hand users demonstrated variable grasp postures and higher reach peak velocities in the complex, but not simple, task. All groups showed decreases in movement duration in the complex task, but only partial-hand users improved in the simple task. These behavioural changes suggest how device level and task may influence prosthesis-use, with relevance to amputation rehabilitation.

Forming tool use representations: a neurophysiological investigation into tool exposure.

Prior work has identified a common left parietofrontal network for storage of tool-related information for various tasks. How these representations become established within this network on the basis of different modes of exposure is unclear. Here, healthy subjects engaged in physical practice (direct exposure) with familiar and unfamiliar tools. A separate group of subjects engaged in video-based observation (indirect exposure) of the same tools to understand how these learning strategies create representations. To assess neural mechanisms engaged for pantomime after different modes of exposure, a pantomime task was performed for both tools while recording neural activation with high-density EEG. Motor planning-related neural activation was evaluated using beta band (13-22 Hz) event-related desynchronization. Hemispheric dominance was assessed, and activation maps were generated to understand topography of activations. Comparison of conditions (effects of tool familiarity and tool exposure) was performed with standardized low-resolution brain electromagnetic tomography. Novel tool pantomime following direct exposure resulted in greater activations of bilateral parietofrontal regions. Activations following indirect training varied by tool familiarity; pantomime of the familiar tool showed greater activations in left parietofrontal areas, whereas the novel tool showed greater activations at right temporoparieto-occipital areas. These findings have relevance to the mechanisms for understanding motor-related behaviors involved in new tools that we have little or no experience with and can extend into advancing theories of tool use motor learning.

Emergence of perceptuomotor relationships during paleolithic stone toolmaking learning: intersections of observation and practice.

Stone toolmaking is a human motor skill which provides the earliest archeological evidence motor skill and social learning. Intentionally shaping a stone into a functional tool relies on the interaction of action observation and practice to support motor skill acquisition. The emergence of adaptive and efficient visuomotor processes during motor learning of such a novel motor skill requiring complex semantic understanding, like stone toolmaking, is not understood. Through the examination of eye movements and motor skill, the current study sought to evaluate the changes and relationship in perceptuomotor processes during motor learning and performance over 90 h of training. Participants' gaze and motor performance were assessed before, during and following training. Gaze patterns reveal a transition from initially high gaze variability during initial observation to lower gaze variability after training. Perceptual changes were strongly associated with motor performance improvements suggesting a coupling of perceptual and motor processes during motor learning.

Theta frequency band activity and attentional mechanisms in visual and proprioceptive demand.

In a companion manuscript we reported reduced electroencephalographic (EEG) activation at traditional sensorimotor areas in knee movements with high levels of task difficulty modulated by varying visual and proprioceptive sensory demands. Given that reduced cortical activity with more complex tasks is counter-intuitive, we suggested that high order cognitive-motor areas may show increased EEG activation to compensate for the observed decrease in sensorimotor regions. To test this hypothesis, we evaluated theta band activation at anterior frontal regions in a secondary analysis of our previous data. Unlike activation at sensorimotor areas, anterior frontal responses increased with each level of task difficulty as modulated by precision of visual targeting and/or proprioceptive demands from adding masses to the leg. Activity was increased as both unimodal visual and proprioceptive requirements became more demanding, but showed greater sensitivity to visual over proprioceptive processing requirements. Each level of bimodal task demands showed increasing activation, which was consistently greater when modulated through visual demands. These results are consistent with our hypothesis of increased contribution of anterior frontal regions for motor control in lower extremity movements with increasing sensory demands and further support different mechanisms for internally and externally guided movement.

Electroencephalographic reactivity to unimodal and bimodal visual and proprioceptive demands in sensorimotor integration.

We used electroencephalography to see how the brain deals with altered sensory processing demands in lower extremity movements. In unimodal conditions, sensory processing demands were altered with subjects performing movement to a small or large visual target, or with a small or large weight to modify proprioception. In bimodal conditions, both weight and targets needed to be met. We assessed activity over primary sensorimotor, premotor and parietal areas before and during knee movements. In unimodal conditions, the primary sensorimotor area showed the least sensitivity to the maximally increased sensory demand in both vision and proprioception, while the premotor region was most sensitive to proprioceptive demands, and the parietal region showed greatest sensitivity to visual demands. In bimodal conditions, intermediate levels of sensory processing demand maximally increased activation at premotor and parietal regions. However, when visual and proprioceptive demands were both maximal, activation decreased and was similar to that seen with the lowest level of sensory processing demand. As behavior was consistent across conditions while activation at these regions decreased, we suggest that additional brain areas, possibly high order cognitive and attentional regions, may be required to augment the function of the traditional sensorimotor network in lower extremity movements with increasingly difficult sensory processing demands.

Reliability of TMS motor evoked potentials in quadriceps of subjects with chronic hemiparesis after stroke.

Transcranial magnetic stimulation (TMS) non-invasively measures excitability of central motor pathways in humans and is used to characterize neuroplasticity after stroke. Using TMS to index lower extremity neuroplasticity after gait rehabilitation requires test-retest reliability. This study assesses the reliability of TMS-derived variables measured at bilateral quadriceps of chronic hemiparetic stroke survivors. Results support using measures of both paretic and nonparetic motor threshold, motor evoked potential (MEP) latencies; and nonparetic MEP amplitudes. Implications for longitudinal research are discussed.

Implicit development of gaze strategies support motor improvements during action encoding training of prosthesis use.

BACKGROUND: Action observation training has been suggested to facilitate motor improvements in the lives of persons with neural injury. Previous studies have shown that for persons with upper limb amputation, matched limb training, where prosthesis users emulate each other, has shown promise above mismatched training where a prosthesis user emulates actions of a person with sound limbs (most commonly that of a therapist). OBJECTIVE: The mechanism underlying the matched limb training benefit is unclear. Gaze strategies may reveal unique patterns between matched and mismatched training which could explain improvements in motor function in matched limb training. METHODS: Twenty persons with sound limbs were trained on how to use a prosthesis simulator using matched or mismatched limb training in a single session. Eye movements were recorded during the training phase. Kinematics were recorded as persons performed the task. RESULTS: Gaze patterns showed differences between the training groups. The mismatched group demonstrated a higher probability of gaze on the path between the start and end of the action, while the matched group demonstrated a significantly higher probability of focusing on the elements of the path of the action and a trend of focusing on the shoulders. Kinematics also revealed overall improvements in motor control for the matched group. CONCLUSIONS: This study proposes a putative mechanism that may explain improvements in matched limb training through shifting gaze strategies. Further work is needed to understand whether implicit visual strategies seen during matched limb training might encourage motor learning during functional training with prostheses.

Role of Interhemispheric Cortical Interactions in Poststroke Motor Function.

Background/Objective. We investigated interhemispheric interactions in stroke survivors by measuring transcranial magnetic stimulation (TMS)-evoked cortical coherence. We tested the effect of TMS on interhemispheric coherence during rest and active muscle contraction and compared coherence in stroke and older adults. We evaluated the relationships between interhemispheric coherence, paretic motor function, and the ipsilateral cortical silent period (iSP). Methods. Participants with (n = 19) and without (n = 14) chronic stroke either rested or maintained a contraction of the ipsilateral hand muscle during simultaneous recordings of evoked responses to TMS of the ipsilesional/nondominant (i/ndM1) and contralesional/dominant (c/dM1) primary motor cortex with EEG and in the hand muscle with EMG. We calculated pre- and post-TMS interhemispheric beta coherence (15-30 Hz) between motor areas in both conditions and the iSP duration during the active condition. Results. During active i/ndM1 TMS, interhemispheric coherence increased immediately following TMS in controls but not in stroke. Coherence during active cM1 TMS was greater than iM1 TMS in the stroke group. Coherence during active iM1 TMS was less in stroke participants and was negatively associated with measures of paretic arm motor function. Paretic iSP was longer compared with controls and negatively associated with clinical measures of manual dexterity. There was no relationship between coherence and. iSP for either group. No within- or between-group differences in coherence were observed at rest. Conclusions. TMS-evoked cortical coherence during hand muscle activation can index interhemispheric interactions associated with poststroke motor function and potentially offer new insights into neural mechanisms influencing functional recovery.

Cortico-cortical networks in patients with ideomotor apraxia as revealed by EEG coherence analysis.

We sought to determine whether coherent networks which circumvent lesioned cortex are seen in patients with ideomotor apraxia (IMA) while performing tool-use pantomimes. Five normal subjects and five patients with IMA (three patients with corticobasal degeneration and two with left hemisphere stroke) underwent 64-channel EEG recording while performing three tool-use pantomimes with their left hand in a self-paced manner. Beta band (20-22 Hz) coherence indicates that normal subjects have a dominant left hemisphere network responsible for praxis preparation, which was absent in patients. Corticobasal degeneration patients showed significant coherence increase between left parietal-right premotor areas. Left hemisphere stroke patients showed significant coherence increases in a right parietofrontal network. The right hemisphere appears to store useable praxis representations in IMA patients with left hemisphere damage.

Preparatory band specific premotor cortical activity differentiates upper and lower extremity movement.

Event related desynchronization (ERD) allows evaluation of brain signals in multiple frequency dimensions. The purpose of this study was to determine left hemispheric non-primary motor cortex differences at varying frequencies of premovement ERD for similar movements by end-effectors of the upper and lower extremities. We recorded 32-channel electroencephalography (EEG) while subjects performed self-paced right ankle dorsiflexion and wrist extension. Electromyography (EMG) was recorded over the tibialis anterior and extensor carpi ulnaris. EEG was analyzed for premovement ERD within the alpha (8-12 Hz), low beta (13-18 Hz) and high beta (18-22 Hz) frequencies over the premotor, motor, and sensory areas of the left and mesial cortex from -1.5 to 0 s before movement. Within the alpha and high beta bands, wrist movements showed limited topography, but greater ERD over posterior premotor cortex areas. Alpha ERD was also significantly greater over the lateral motor cortex for wrist movements. In the low beta band, wrist movements provided extensive ERD differences to include the left motor and mesial/lateral premotor areas, whereas ankle movements showed only limited ERD activity. Overall, alpha and high beta activity demonstrated distinctions that are consistent with mapping of wrist and ankle representations over the sensorimotor strip, whereas the low beta representation demonstrated the clearest distinctions between the limbs over widespread brain areas, particularly the lateral premotor cortex. This suggests limited leg premovement activity at the dorsolateral premotor cortex. Low beta ERD may be reflect joint or limb specific preparatory activity in the premotor area. Further work is required to better evaluate the extent of this low beta activity for multiple comparative joints.

The Role of Attention and Saccades on Parietofrontal Encoding of Contextual and Grasp-specific Affordances of Tools: An ERP Study.

The ability to recognize a tool's affordances (how a spoon should be appropriately grasped and used), is vital for daily life. Prior research has identified parietofrontal circuits, including mirror neurons, to be critical in understanding affordances. However, parietofrontal action-encoding regions receive extensive visual input and are adjacent to parietofrontal attention control networks. It is unclear how eye movements and attention modulate parietofrontal encoding of affordances. To address this issue, scenes depicting tools in different use-contexts and grasp-postures were presented to healthy subjects across two experiments, with stimuli durations of 100 ms or 500 ms. The 100-ms experiment automatically restricted saccades and required covert attention, while the 500-ms experiment allowed overt attention. The two experiments elicited similar behavioral decisions on tool-use correctness and isolated the influence of attention on parietofrontal activity. Parietofrontal ERPs (P600) distinguishing tool-use contexts (e.g., spoon-yogurt vs. spoon-ball) were similar in both experiments. Conversely, parietofrontal ERPs distinguishing tool-grasps were characterized by posterior to frontal N130-N200 ERPs in the 100-ms experiment and by saccade-perturbed N130-N200 ERPs, frontal N400 and parietal P500 in the 500-ms experiment. Particularly, only overt gaze toward the hand-tool interaction engaged mirror neurons (frontal N400) when discerning grasps that manipulate but not functionally use a tool - (grasp bowl rather than stem of spoon). Results here detail the first human electrophysiological evidence on how attention selectively modulates multiple parietofrontal grasp-perception circuits, especially the mirror neuron system, while unaffecting parietofrontal encoding of tool-use contexts. These results are pertinent to neurophysiological models of affordances that typically neglect the role of attention in action perception.