Sheila M. Schindler-Ivens

Observation of Amounts of Movement Practice Provided During Stroke Rehabilitation

UNLABELLED Lang CE, MacDonald JR, Reisman DS, Boyd L, Jacobson Kimberley T, Schindler-Ivens SM, Hornby TG, Ross SA, Scheets PL. Observation of amounts of movement practice provided during stroke rehabilitation. OBJECTIVE To investigate how much movement practice occurred during stroke rehabilitation, and what factors might influence doses of practice provided. DESIGN Observational survey of stroke therapy sessions. SETTING Seven inpatient and outpatient rehabilitation sites. PARTICIPANTS We observed a convenience sample of 312 physical and occupational therapy sessions for people with stroke. INTERVENTIONS Not applicable. MAIN OUTCOME MEASURES We recorded numbers of repetitions in specific movement categories and data on potential modifying factors (patient age, side affected, time since stroke, FIM item scores, years of therapist experience). Descriptive statistics were used to characterize amounts of practice. Correlation and regression analyses were used to determine whether potential factors were related to the amount of practice in the 2 important categories of upper extremity functional movements and gait steps. RESULTS Practice of task-specific, functional upper extremity movements occurred in 51% of the sessions that addressed upper limb rehabilitation, and the average number of repetitions/session was 32 (95% confidence interval [CI]=20-44). Practice of gait occurred in 84% of sessions that addressed lower limb rehabilitation and the average number of gait steps/session was 357 (95% CI=296-418). None of the potential factors listed accounted for significant variance in the amount of practice in either of these 2 categories. CONCLUSIONS The amount of practice provided during poststroke rehabilitation is small compared with animal models. It is possible that current doses of task-specific practice during rehabilitation are not adequate to drive the neural reorganization needed to promote function poststroke optimally.

A novel technique for examining human brain activity associated with pedaling using fMRI.

Advances in neural imaging technologies, such as functional magnetic resonance imaging (fMRI), have made it possible to obtain images of human brain activity during motor tasks. However, technical challenges have made it difficult to image the brain during multijoint lower limb movements like those involved in locomotion. We developed an MR compatible pedaling device and recorded human brain activity associated with rhythmic, alternating flexion and extension of the lower extremities. Ten volunteers pedaled at 30 RPM while recording fMRI signals in a GE 3T short bore MR scanner. We utilized a block design consisting of 3 runs of pedaling, each lasting 4 min. In a single run, subjects pedaled for 30 s and then rested for 30 s. This sequence was repeated 4 times. Conventional fMRI processing techniques, that correlate the entire BOLD signal with standard model, did not extract physiologically meaningful signal, likely due to magnetic field distortion caused by leg movement. Hence, we examined only the portion of the blood-oxygen-level dependent (BOLD) signal during movement-free periods. This technique takes advantage of the delayed nature of the BOLD signal and fits the falling portion of the signal after movement has stopped with a standard model. Using this approach, we observed physiologically plausible brain activity patterns associated with pedaling in the primary and secondary sensory and motor cortices and the cerebellum. To our knowledge, this is the first time that human brain activity associated with pedaling has been recorded with fMRI. This technique may be useful for advancing our understanding of supraspinal control of locomotor-like movements in health and disease.

EEG during pedaling: Evidence for cortical control of locomotor tasks

OBJECTIVE This study characterized the brain electrical activity during pedaling, a locomotor-like task, in humans. We postulated that phasic brain activity would be associated with active pedaling, consistent with a cortical role in locomotor tasks. METHODS Sixty four channels of electroencephalogram (EEG) and 10 channels of electromyogram (EMG) data were recorded from 10 neurologically-intact volunteers while they performed active and passive (no effort) pedaling on a custom-designed stationary bicycle. Ensemble averaged waveforms, 2 dimensional topographic maps and amplitude of the β (13-35 Hz) frequency band were analyzed and compared between active and passive trials. RESULTS The peak-to-peak amplitude (peak positive-peak negative) of the EEG waveform recorded at the Cz electrode was higher in the passive than the active trials (p < 0.01). β-band oscillations in electrodes overlying the leg representation area of the cortex were significantly desynchronized during active compared to the passive pedaling (p < 0.01). A significant negative correlation was observed between the average EEG waveform for active trials and the composite EMG (summated EMG from both limbs for each muscle) of the rectus femoris (r = -0.77, p < 0.01) the medial hamstrings (r = -0.85, p < 0.01) and the tibialis anterior (r = -0.70, p < 0.01) muscles. CONCLUSIONS These results demonstrated that substantial sensorimotor processing occurs in the brain during pedaling in humans. Further, cortical activity seemed to be greatest during recruitment of the muscles critical for transitioning the legs from flexion to extension and vice versa. SIGNIFICANCE This is the first study demonstrating the feasibility of EEG recording during pedaling, and owing to similarities between pedaling and bipedal walking, may provide valuable insight into brain activity during locomotion in humans.

Between-day reliability of upper extremity H-reflexes

H-reflexes are useful for evaluating the group Ia monosynaptic reflex excitability in the lower and upper extremities (UEs). However, there is no established between-day protocol for measuring H-reflex excitability in the UE extensor carpi radialis longus (ECRL). The purpose of this study was to develop a reliable protocol to measure the H-reflex excitability between-days for the ECRL, and the antagonist muscle, the flexor carpi radialis (FCR). H-reflex recruitment curves were recorded from eight healthy young subjects over 3 consecutive days in both muscles. Variables associated with the H-reflex excitability were measured: (a) maximum amplitude (Hmax); (b) gain (HGN); (c) threshold (HTH, visHTH, and sdHTH). All variables were normalized with respect to the M-wave. Within individual muscles, there were no statistically significant differences between-days for the group (p>0.05) and variables showed fair to good reliability (ICC=0.57-0.99). This method of reliably measuring H-reflex excitability within UE muscles will be useful for investigating the effects of pathology and rehabilitation on monosynaptic reflexes.

Reciprocal inhibition post-stroke is related to reflex excitability and movement ability

OBJECTIVE Decreased reciprocal inhibition (RI) of motor neurons may contribute to spasticity after stroke. However, decreased RI is not a uniform observation among stroke survivors, suggesting that this spinal circuit may be influenced by other stroke-related characteristics. The purpose of this study was to measure RI post-stroke and to examine the relationship between RI and other features of stroke. METHODS RI was examined in 15 stroke survivors (PAR) and 10 control subjects by quantifying the effect of peroneal nerve stimulation on soleus H-reflex amplitude. The relationship between RI and age, time post-stroke, lesion side, walking velocity, Fugl-Meyer, Ashworth, and Achilles reflex scores was examined. RESULTS RI was absent and replaced by reciprocal facilitation in 10 of 15 PAR individuals. Reciprocal facilitation was associated with low Fugl-Meyer scores and slow walking velocities but not with hyperactive Achilles tendon reflexes. There was no relationship between RI or reciprocal facilitation and time post-stroke, lesion side, or Ashworth score. CONCLUSIONS Decreased RI is not a uniform finding post-stroke and is more closely related to walking ability and movement impairment than to spasticity. SIGNIFICANCE Phenomena other than decreased RI may contribute to post-stroke spasticity.

White matter structural connectivity is associated with sensorimotor function in stroke survivors

Purpose Diffusion tensor imaging (DTI) provides functionally relevant information about white matter structure. Local anatomical connectivity information combined with fractional anisotropy (FA) and mean diffusivity (MD) may predict functional outcomes in stroke survivors. Imaging methods for predicting functional outcomes in stroke survivors are not well established. This work uses DTI to objectively assess the effects of a stroke lesion on white matter structure and sensorimotor function. Methods A voxel-based approach is introduced to assess a stroke lesions global impact on motor function. Anatomical T1-weighted and diffusion tensor images of the brain were acquired for nineteen subjects (10 post-stroke and 9 age-matched controls). A manually selected volume of interest was used to alleviate the effects of stroke lesions on image registration. Images from all subjects were registered to the images of the control subject that was anatomically closest to Talairach space. Each subjects transformed image was uniformly seeded for DTI tractography. Each seed was inversely transformed into the individual subject space, where DTI tractography was conducted and then the results were transformed back to the reference space. A voxel-wise connectivity matrix was constructed from the fibers, which was then used to calculate the number of directly and indirectly connected neighbors of each voxel. A novel voxel-wise indirect structural connectivity (VISC) index was computed as the average number of direct connections to a voxels indirect neighbors. Voxel-based analyses (VBA) were performed to compare VISC, FA, and MD for the detection of lesion-induced changes in sensorimotor function. For each voxel, a t-value was computed from the differences between each stroke brain and the 9 controls. A series of linear regressions was performed between Fugl-Meyer (FM) assessment scores of sensorimotor impairment and each DTI metrics log number of voxels that differed from the control group. Results Correlation between the logarithm of the number of significant voxels in the ipsilesional hemisphere and total Fugl-Meyer score was moderate for MD (R2 = 0.512), and greater for VISC (R2 = 0.796) and FA (R2 = 0.674). The slopes of FA (p = 0.0036), VISC (p = 0.0005), and MD (p = 0.0199) versus the total FM score were significant. However, these correlations were driven by the upper extremity motor component of the FM score (VISC: R2 = 0.879) with little influence of the lower extremity motor component (FA: R2 = 0.177). Conclusion The results suggest that a voxel-wise metric based on DTI tractography can predict upper extremity sensorimotor function of stroke survivors, and that supraspinal intraconnectivity may have a less dominant role in lower extremity function.

Pedaling alters the excitability and modulation of vastus medialis H-reflexes after stroke

OBJECTIVE Individuals post-stroke display abnormal Group Ia reflex excitability. Pedaling has been shown to reduce Group Ia reflexes and to normalize the relationship between EMG and reflex amplitude in the paretic soleus (SO). The purpose of this study was to determine whether these changes extend to the paretic quadriceps. METHODS H-reflexes were used to examine Group Ia reflex excitability of the vastus medialis (VM). H-reflexes were elicited in paretic (n=13) and neurologically intact (n=13) individuals at 11 positions in the pedaling cycle and during static knee extension at comparable limb positions and levels of VM EMG. RESULTS VM H-reflexes were abnormally elevated in the paretic limb of stroke survivors. During static muscle activation, H-reflex amplitude did not change with the level of background VM activity. Pedaling reduced the amplitude of paretic VM H-reflexes and restored the normal relationship between VM EMG and H-reflex amplitude. CONCLUSIONS Pedaling-induced changes in Group Ia reflex excitability that have been reported for the paretic SO are evident in the paretic VM. Pedaling may have a generalized effect on lower extremity Group Ia reflexes post-stroke. SIGNIFICANCE Pedaling may be therapeutic for reducing Group Ia reflexes after stroke.

Lower Extremity Passive Range of Motion in Community-Ambulating Stroke Survivors

Background: Physical therapists may prescribe stretching exercises for individuals with stroke to improve joint integrity and to reduce the risk of secondary musculoskeletal impairment. While deficits in passive range of motion (PROM) exist in stroke survivors with severe hemiparesis and spasticity, the extent to which impaired lower extremity PROM occurs in community-ambulating stroke survivors remains unclear. This study compared lower extremity PROM in able-bodied individuals and independent community-ambulatory stroke survivors with residual stroke-related neuromuscular impairments. Our hypothesis was that the stroke group would show decreased lower extremity PROM in the paretic but not the nonparetic side and that decreased PROM would be associated with increased muscle stiffness and decreased muscle length. Methods: Individuals with chronic poststroke hemiparesis who reported the ability to ambulate independently in the community (n = 17) and age-matched control subjects (n = 15) participated. PROM during slow (5 degrees/sec) hip extension, hip flexion, and ankle dorsiflexion was examined bilaterally using a dynamometer that measured joint position and torque. The maximum angular position of the joint (ANGmax), torque required to achieve ANGmax (Tmax), and mean joint stiffness (K) were measured. Comparisons were made between able-bodied and paretic and able-bodied and nonparetic limbs. Results: Contrary to our expectations, between-group differences in ANGmax were observed only during hip extension in which ANGmax was greater bilaterally in people post-stroke compared to control subjects (P ≤ 0.05; stroke = 13 degrees, able-bodied = −1 degree). Tmax, but not K, was also significantly higher during passive hip extension in paretic and nonparetic limbs compared to control limbs (P ≤ 0.05; stroke = 40 Nm, able-bodied = 29 Nm). Compared to the control group, Tmax was increased during hip flexion in the paretic and nonparetic limbs of post-stroke subjects (P ≤ 0.05, stroke = 25 Nm, able-bodied = 18 Nm). K in the nonparetic leg was also increased during hip flexion (P ≤ 0.05, nonparetic = 0.52 Nm/degree, able-bodied = 0.37 Nm/degree.) Conclusion: This study demonstrates that community-ambulating stroke survivors with residual neuromuscular impairments do not have decreased lower extremity PROM caused by increased muscle stiffness or decreased muscle length. In fact, the population of stroke survivors examined here appears to have more hip extension PROM than age-matched able-bodied individuals. The clinical implications of these data are important and suggest that lower extremity PROM may not interfere with mobility in community-ambulating stroke survivors. Hence, physical therapists may choose to recommend activities other than stretching exercises for stroke survivors who are or will become independent community ambulators.

A novel fMRI paradigm suggests that pedaling-related brain activation is altered after stroke

The purpose of this study was to examine the feasibility of using functional magnetic resonance imaging (fMRI) to measure pedaling-related brain activation in individuals with stroke and age-matched controls. We also sought to identify stroke-related changes in brain activation associated with pedaling. Fourteen stroke and 12 control subjects were asked to pedal a custom, MRI-compatible device during fMRI. Subjects also performed lower limb tapping to localize brain regions involved in lower limb movement. All stroke and control subjects were able to pedal while positioned for fMRI. Two control subjects were withdrawn due to claustrophobia, and one control data set was excluded from analysis due to an incidental finding. In the stroke group, one subject was unable to enter the gantry due to excess adiposity, and one stroke data set was excluded from analysis due to excessive head motion. Consequently, 81% of subjects (12/14 stroke, 9/12 control) completed all procedures and provided valid pedaling-related fMRI data. In these subjects, head motion was ≤3 mm. In both groups, brain activation localized to the medial aspect of M1, S1, and Brodmann’s area 6 (BA6) and to the cerebellum (vermis, lobules IV, V, VIII). The location of brain activation was consistent with leg areas. Pedaling-related brain activation was apparent on both sides of the brain, with values for laterality index (LI) of –0.06 (0.20) in the stroke cortex, 0.05 (±0.06) in the control cortex, 0.29 (0.33) in the stroke cerebellum, and 0.04 (0.15) in the control cerebellum. In the stroke group, activation in the cerebellum – but not cortex – was significantly lateralized toward the damaged side of the brain (p = 0.01). The volume of pedaling-related brain activation was smaller in stroke as compared to control subjects. Differences reached statistical significance when all active regions were examined together [p = 0.03; 27,694 (9,608) μL stroke; 37,819 (9,169) μL control]. When individual regions were examined separately, reduced brain activation volume reached statistical significance in BA6 [p = 0.04; 4,350 (2,347) μL stroke; 6,938 (3,134) μL control] and cerebellum [p = 0.001; 4,591 (1,757) μL stroke; 8,381 (2,835) μL control]. Regardless of whether activated regions were examined together or separately, there were no significant between-group differences in brain activation intensity [p = 0.17; 1.30 (0.25)% stroke; 1.16 (0.20)% control]. Reduced volume in the stroke group was not observed during lower limb tapping and could not be fully attributed to differences in head motion or movement rate. There was a tendency for pedaling-related brain activation volume to increase with increasing work performed by the paretic limb during pedaling (p = 0.08, r = 0.525). Hence, the results of this study provide two original and important contributions. First, we demonstrated that pedaling can be used with fMRI to examine brain activation associated with lower limb movement in people with stroke. Unlike previous lower limb movements examined with fMRI, pedaling involves continuous, reciprocal, multijoint movement of both limbs. In this respect, pedaling has many characteristics of functional lower limb movements, such as walking. Thus, the importance of our contribution lies in the establishment of a novel paradigm that can be used to understand how the brain adapts to stroke to produce functional lower limb movements. Second, preliminary observations suggest that brain activation volume is reduced during pedaling post-stroke. Reduced brain activation volume may be due to anatomic, physiology, and/or behavioral differences between groups, but methodological issues cannot be excluded. Importantly, brain action volume post-stroke was both task-dependent and mutable, which suggests that it could be modified through rehabilitation. Future work will explore these possibilities.

A pilot study to measure upper extremity H-reflexes following neuromuscular electrical stimulation therapy after stroke

Upper extremity (UE) hemiparesis persists after stroke, limiting hand function. Neuromuscular electrical stimulation (NMES) is an effective intervention to improve UE recovery, although the underlying mechanisms are not fully understood. Our objective was to establish a reliable protocol to measure UE agonist-antagonist forearm monosynaptic reflexes in a pilot study to determine if NMES improves wrist function after stroke. We established the between-day reliability of the H-reflex in the extensor carpi radialis longus (ECRL) and flexor carpi radialis (FCR) musculature for individuals with prior stroke (n=18). The same-day generation of ECRL/FCR H-reflex recruitment curves was well tolerated, regardless of age or UE spasticity. The between-day reliability of the ECRL H-reflex was enhanced above FCR, similar to healthy subjects [20], with the Hmax the most reliable parameter quantified in both muscles. H-reflex and functional measures following NMES show the potential for NMES-induced increases in ECRL Hmax, but confirmation requires a larger clinical study. Our initial results support the safe, easy, and efficacious use of in-home NMES, and establish a potential method to measure UE monosynaptic reflexes after stroke.