Jennifer A. Semrau

Robotic Identification of Kinesthetic Deficits After Stroke

Background and Purpose— Kinesthesia, the sense of body motion, is essential to proper control and execution of movement. Despite its importance for activities of daily living, no current clinical measures can objectively measure kinesthetic deficits. The goal of this study was to use robotic technology to quantify prevalence and severity of kinesthetic deficits of the upper limb poststroke. Methods— Seventy-four neurologically intact subjects and 113 subjects with stroke (62 left-affected, 51 right-affected) performed a robot-based kinesthetic matching task with vision occluded. The robot moved the most affected arm at a preset speed, direction, and magnitude. Subjects were instructed to mirror-match the movement with their opposite arm (active arm). Results— A large number of subjects with stroke were significantly impaired on measures of kinesthesia. We observed impairments in ability to match movement direction (69% and 49% impaired for left- and right-affected subjects, respectively) and movement magnitude (42% and 31%). We observed impairments to match movement speed (32% and 27%) and increased response latencies (48% and 20%). Movement direction errors and response latencies were related to clinical measures of function, motor recovery, and dexterity. Conclusions— Using a robotic approach, we found that 61% of acute stroke survivors (n=69) had kinesthetic deficits. Additionally, these deficits were highly related to existing clinical measures, suggesting the importance of kinesthesia in day-to-day function. Our methods allow for more sensitive, accurate, and objective identification of kinesthetic deficits after stroke. With this information, we can better inform clinical treatment strategies to improve poststroke rehabilitative care and outcomes.

Examining Differences in Patterns of Sensory and Motor Recovery After Stroke With Robotics

Background and Purpose— Developing a better understanding of the trajectory and timing of stroke recovery is critical for developing patient-centered rehabilitation approaches. Here, we quantified proprioceptive and motor deficits using robotic technology during the first 6 months post stroke to characterize timing and patterns in recovery. We also make comparisons of robotic assessments to traditional clinical measures. Methods— One hundred sixteen subjects with unilateral stroke were studied at 4 time points: 1, 6, 12, and 26 weeks post stroke. Subjects performed robotic assessments of proprioceptive (position sense and kinesthesia) and motor function (unilateral reaching task and bimanual object hit task), as well as several clinical measures (Functional Independence Measure, Purdue Pegboard, and Chedoke-McMaster Stroke Assessment). Results— One week post stroke, many subjects displayed proprioceptive (48% position sense and 68% kinesthesia) and motor impairments (80% unilateral reaching and 85% bilateral movement). Interindividual recovery on robotic measures was highly variable. However, we characterized recovery as early (normal by 6 weeks post stroke), late (normal by 26 weeks post stroke), or incomplete (impaired at 26 weeks post stroke). Proprioceptive and motor recovery often followed different timelines. Across all time points, robotic measures were correlated with clinical measures. Conclusions— These results highlight the need for more sensitive, targeted identification of sensory and motor deficits to optimize rehabilitation after stroke. Furthermore, the trajectory of recovery for some individuals with mild to moderate stroke may be much longer than previously considered.

Anatomical correlates of proprioceptive impairments following acute stroke: A case series

BACKGROUND Proprioception is the sensation of position and movement of our limbs and body in space. This sense is important for performing smooth coordinated movements and is impaired in approximately 50% of stroke survivors. In the present case series we wanted to determine how discrete stroke lesions to areas of the brain thought to be critical for somatosensation (thalamus, posterior limb of internal capsule, primary somatosensory cortex and posterior parietal cortex) would affect position sense and kinesthesia in the acute stages post-stroke. Given the known issues with standard clinical measures of proprioception (i.e. poor sensitivity and reliability) we used more modern quantitative robotic assessments to measure proprioception. METHODS Neuroimaging (MRI, n=10 or CT, n=2) was performed on 12 subjects 2-10 days post-stroke. Proprioception was assessed using a KINARM robot within the same time frame. Visually guided reaching was also assessed to allow us to compare and contrast proprioception with visuomotor performance. RESULTS AND CONCLUSIONS Proprioceptive impairments were observed in 7 of 12 subjects. Thalamic lesions (n=4) were associated with position sense (n=1) or position sense and kinesthesia (n=1) impairments. Posterior limb of the internal capsule lesions (n=4) were associated with primarily position sense (n=1) or kinesthesia (n=2) impairments. Lesions affecting primary somatosensory cortex and posterior parietal cortex (n=2) were associated with significant position sense and kinesthesia impairments. All subjects with damage to hypothesized structures displayed impairments with performance on the visually guided reaching task. Across the proprioceptive tasks, we saw that position sense and kinesthesia were impaired to differing degrees, suggesting a potential dissociation between these two components of proprioception.

Relationship Between Visuospatial Neglect and Kinesthetic Deficits After Stroke

Background. After stroke, visuospatial and kinesthetic (sense of limb motion) deficits are common, occurring in approximately 30% and 60% of individuals, respectively. Although both types of deficits affect aspects of spatial processing necessary for daily function, few studies have investigated the relationship between these 2 deficits after stroke. Objective. We aimed to characterize the relationship between visuospatial and kinesthetic deficits after stroke using the Behavioral Inattention Test (BIT) and a robotic measure of kinesthetic function. Methods. Visuospatial attention (using the BIT) and kinesthesia (using robotics) were measured in 158 individuals an average of 18 days after stroke. In the kinesthetic matching task, the robot moved the participant’s stroke-affected arm at a preset direction, speed, and magnitude. Participants mirror-matched the robotic movement with the less/unaffected arm as soon as they felt movement in their stroke affected arm. Results. We found that participants with visuospatial inattention (neglect) had impaired kinesthesia 100% of the time, whereas only 59% of participants without neglect were impaired. For those without neglect, we observed that a higher percentage of participants with lower but passing BIT scores displayed impaired kinesthetic behavior (78%) compared with those participants who scored perfect or nearly perfect on the BIT (49%). Conclusions. The presence of visuospatial neglect after stroke is highly predictive of the presence of kinesthetic deficits. However, the presence of kinesthetic deficits does not necessarily always indicate the presence of visuospatial neglect. Our findings highlight the importance of assessment and treatment of kinesthetic deficits after stroke, especially in patients with visuospatial neglect.

Robotic Quantification of Position Sense in Children With Perinatal Stroke

Background. Perinatal stroke is the leading cause of hemiparetic cerebral palsy. Motor deficits and their treatment are commonly emphasized in the literature. Sensory dysfunction may be an important contributor to disability, but it is difficult to measure accurately clinically. Objective. Use robotics to quantify position sense deficits in hemiparetic children with perinatal stroke and determine their association with common clinical measures. Methods. Case-control study. Participants were children aged 6 to 19 years with magnetic resonance imaging–confirmed unilateral perinatal arterial ischemic stroke or periventricular venous infarction and symptomatic hemiparetic cerebral palsy. Participants completed a position matching task using an exoskeleton robotic device (KINARM). Position matching variability, shift, and expansion/contraction area were measured with and without vision. Robotic outcomes were compared across stroke groups and controls and to clinical measures of disability (Assisting Hand Assessment) and sensory function. Results. Forty stroke participants (22 arterial, 18 venous, median age 12 years, 43% female) were compared with 60 healthy controls. Position sense variability was impaired in arterial (6.01 ± 1.8 cm) and venous (5.42 ± 1.8 cm) stroke compared to controls (3.54 ± 0.9 cm, P < .001) with vision occluded. Impairment remained when vision was restored. Robotic measures correlated with functional disability. Sensitivity and specificity of clinical sensory tests were modest. Conclusions. Robotic assessment of position sense is feasible in children with perinatal stroke. Impairment is common and worse in arterial lesions. Limited correction with vision suggests cortical sensory network dysfunction. Disordered position sense may represent a therapeutic target in hemiparetic cerebral palsy.

Lesion Sites Associated with Allocentric and Egocentric Visuospatial Neglect in Acute Stroke

Visuospatial neglect is a disorder that can often result from stroke and is characterized by an inability to attend to contralesional stimuli. Two common subtypes include allocentric (object-centered) neglect and egocentric (viewer-centered) neglect. In allocentric neglect, spatial inattention is localized to the contralesional side of an object regardless of its relative position to the observer. In egocentric neglect, spatial inattention is localized to the contralesional side of the individuals midline. The neuroanatomical correlates of each subtype are unknown. However, recent work has suggested that damage to temporal, inferior parietal, and occipital areas may result in allocentric neglect and that damage to frontoparietal areas may result in egocentric neglect. We used voxel-based lesion-symptom mapping (VLSM) to compare lesion location to behavioral performance on the conventional six subtests of the Behavioral Inattention Test (BIT) in 62 subjects with acute right hemisphere ischemic stroke. Results identified an anatomical dissociation in lesion location between subjects with neglect based on poor performance on allocentric tests (line bisection, copying, and drawing tasks) and on egocentric tests (star, letter, and line cancellation). VLSM analyses revealed that poor performance on the allocentric tests was associated with lesions to the superior and inferior parietal cortices, and the superior and middle temporal gyri. In contrast, poor performance on the egocentric tests was associated with lesions in the precentral gyrus, middle frontal gyrus, insula, and putamen. Interestingly, the letter cancellation test and average performance on egocentric tests were associated with frontal and parietal lesions. Some of these parietal lesion locations overlapped with lesion locations associated with allocentric neglect. These findings are consistent with suggestions that damage to temporal and parietal areas is more associated with allocentric neglect and damage to frontal lobe areas is more associated with egocentric neglect.

Central perception of position sense involves a distributed neural network - Evidence from lesion-behavior analyses.

It is well established that proprioceptive inputs from the periphery are important for the constant update of arm position for perception and guiding motor action. The degree to which we are consciously aware of the position of our limb depends on the task. Our understanding of the central processing of position sense is rather limited, largely based on findings in animals and individual human case studies. The present study used statistical lesion-behavior analysis and an arm position matching task to investigate position sense in a large sample of subjects after acute stroke. We excluded subjects who performed abnormally on clinical testing or a robotic visually guided reaching task with their matching arm in order to minimize the potential confound of ipsilesional impairment. Our findings revealed that a number of regions are important for processing position sense and include the posterior parietal cortex, the transverse temporal gyrus, and the arcuate fasciculus. Further, our results revealed that position sense has dissociable components - spatial variability, perceived workspace area, and perceived workspace location. Each component is associated with unique neuroanatomical correlates. These findings extend the current understanding of the neural processing of position sense and identify some brain areas that are not classically associated with proprioception.

Robotic Characterization of Ipsilesional Motor Function in Subacute Stroke

Background. Poststroke impairments of the ipsilesional arm are often discussed, but rarely receive focused rehabilitation. Ipsilesional deficits may affect daily function and although many studies have investigated them in chronic stroke, few characterizations have been made in the subacute phase. Furthermore, most studies have quantified ipsilesional deficits using clinical measures that can fail to detect subtle, but important deficits in motor function. Objective. We aimed to quantify reaching deficits of the contra- and ipsilesional limbs in the subacute phase poststroke. Methods. A total of 227 subjects with first-time, unilateral stroke completed a unilateral assessment of motor function (visually guided reaching) using a KINARM robot. Subjects completed the task with both the ipsi- and contralesional arms. Subjects were assessed on a variety of traditional clinical measures (Functional Independence Measure, Chedoke-McMaster Stroke Assessment, Purdue Pegboard, Behavioral Inattention Test) to compare with robotic measures of motor function. Results. Ipsilesional deficits were common and occurred in 37% (n = 84) of subjects. Impairments of the ipsilesional and contralesional arm were weakly to moderately correlated on robotic measures. Magnitude of impairment of the contralesional arm was similar for subjects with and without ipsilesional deficits. Furthermore, we found that a higher percentage of subjects with right-hemisphere stroke had ipsilesional deficits and more subjects with left-hemisphere subcortical strokes did not have ipsilesional deficits. Conclusions. Magnitude of contralesional impairment and lesion location may be poor predictors of individuals with ipsilesional impairments after stroke. Careful characterization of ipsilesional deficits could identify individuals who may benefit from rehabilitation of the less affected arm.

Sensory tractography and robot‐quantified proprioception in hemiparetic children with perinatal stroke

Perinatal stroke causes most hemiparetic cerebral palsy, resulting in lifelong disability. We have demonstrated the ability of robots to quantify sensory dysfunction in hemiparetic children but the relationship between such deficits and sensory tract structural connectivity has not been explored. It was aimed to characterize the relationship between the dorsal column medial lemniscus (DCML) pathway connectivity and proprioceptive dysfunction in children with perinatal stroke. Twenty‐nine participants (6–19 years old) with MRI‐classified, unilateral perinatal ischemic stroke (14 arterial, 15 venous), and upper extremity deficits were recruited from a population‐based cohort and compared with 21 healthy controls. Diffusion tensor imaging (DTI) defined DCML tracts and five diffusion properties were quantified: fractional anisotropy (FA), mean, radial, and axial diffusivities (MD, RD, AD), and fiber count. A robotic exoskeleton (KINARM) tested upper limb proprioception in an augmented reality environment. Correlations between robotic measures and sensory tract diffusion parameters were evaluated. Lesioned hemisphere sensory tracts demonstrated lower FA and higher MD, RD, and AD compared with the non‐dominant hemisphere of controls. Dominant (contralesional) hemisphere tracts were not different from controls. Both arterial and venous stroke groups demonstrated impairments in proprioception that correlated with lesioned hemisphere DCML tract diffusion properties. Sensory tract connectivity is altered in the lesioned hemisphere of hemiparetic children with perinatal stroke. A correlation between lesioned DCML tract diffusion properties and robotic proprioceptive measures suggests clinical relevance and a possible target for therapeutic intervention. Hum Brain Mapp 38:2424–2440, 2017.

Disruption in proprioception from long-term thalamic deep brain stimulation: a pilot study

Deep brain stimulation (DBS) is an excellent treatment for tremor and is generally thought to be reversible by turning off stimulation. For tremor, DBS is implanted in the ventrointermedius (Vim) nucleus of the thalamus, a region that relays proprioceptive information for movement sensation (kinaesthesia). Gait disturbances have been observed with bilateral Vim DBS, but the long-term effects on proprioceptive processing are unknown. We aimed to determine whether Vim DBS surgical implantation or stimulation leads to proprioceptive deficits in the upper limb. We assessed two groups of tremor subjects on measures of proprioception (kinaesthesia, position sense) and motor function using a robotic exoskeleton. In the first group (Surgery), we tested patients before and after implantation of Vim DBS, but before DBS was turned on to determine if proprioceptive deficits were inherent to tremor or caused by DBS implantation. In the second group (Stim), we tested subjects with chronically implanted Vim DBS ON and OFF stimulation. Compared to controls, there were no proprioceptive deficits before or after DBS implantation in the Surgery group. Surprisingly, those that received chronic long-term stimulation (LT-stim, 3–10 years) displayed significant proprioceptive deficits ON and OFF stimulation not present in subjects with chronic short-term stimulation (ST-stim, 0.5–2 years). LT-stim had significantly larger variability and reduced workspace area during the position sense assessment. During the kinesthetic assessment, LT-stim made significantly larger directional errors and consistently underestimated the speed of the robot, despite generating normal movement speeds during motor assessment. Chronic long-term Vim DBS may potentially disrupt proprioceptive processing, possibly inducing irreversible plasticity in the Vim nucleus and/or its network connections. Our findings in the upper limb may help explain some of the gait disturbances seen by others following Vim DBS.