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ORIGINAL ARTICLE
Use of Visual Force Feedback to Improve Digit Force Direction During Pinch Grip in Persons With Stroke: A Pilot Study Na Jin Seo, PhD, Heidi W. Fischer, MS, OT, Ross A. Bogey, DO, William Z. Rymer, MD, PhD, Derek G. Kamper, PhD ABSTRACT. Seo NJ, Fischer HW, Bogey RA, Rymer WZ, Kamper DG. Use of visual force feedback to improve digit force direction during pinch grip in persons with stroke: a pilot study. Arch Phys Med Rehabil 2011;92:24-30. Objective: To investigate whether visual feedback of digit force directions for the index fingertip and thumb tip during repeated practice of grip force production can correct the digit force directions for persons with stroke during grip assessments. Following stroke, the paretic fingers generate digit forces with a higher than normal proportion of shear force to compression force during grip. This misdirected digit force may lead to finger-object slip and failure to stably grasp an object. Design: A case series. Setting: Laboratory. Participants: Persons (N⫽11) with severe chronic hand impairment after stroke. Interventions: Four training sessions during which participants practiced directing the index finger and thumb forces in various target directions during pinch using visual feedback. Main Outcome Measure: Digit force direction during pinch and clinical hand function scores were measured before and immediately after the training. Results: Study participants were able to redirect the digit force closer to the direction perpendicular to the object surface and increase their hand function scores after training. The mean ratio of the shear force to the normal force decreased from 58% to 41% (SD, 17%), the mean Box and Block Test score increased from 1.4 to 3.4 (SD, 2.0), and the mean Action Research Arm Test score increased from 10.8 to 12.1 (SD, 1.3) (P⬍.05 for all 3 measures). Conclusions: Repeated practice of pinch with visual feedback of force direction improved grip force control in persons with stroke. Visual feedback of pinch forces may prove valuable as a rehabilitation paradigm for improving hand function.
From the Department of Industrial Engineering, University of WisconsinMilwaukee, Milwaukee, WI (Seo); Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, IL (Seo, Fischer, Bogey, Rymer, Kamper); Department of Physical Medicine and Rehabilitation, Northwestern University, Chicago, IL (Bogey, Rymer); and Department of Biomedical Engineering, Illinois Institute of Technology, Chicago, IL (Kamper). Presented in part to the Society for Neuroscience, October 21, 2009, Chicago, IL. Supported by the Coleman Foundation and the American Heart Association (grant no. 0920067G). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Correspondence to Na Jin Seo, PhD, Dept of Industrial Engineering, University of Wisconsin-Milwaukee, PO Box 413, Milwaukee, WI 53201, e-mail:
[email protected]. Reprints are not available from the authors. Published online November 19, 2010 at www.archives-pmr.org 0003-9993/11/9201-00164$36.00/0 doi:10.1016/j.apmr.2010.08.016
Arch Phys Med Rehabil Vol 92, January 2011
Key Words: Biofeedback, psychology; Fingers; Hand; Rehabilitation; Feedback, sensory; Stroke; Touch. © 2011 by the American Congress of Rehabilitation Medicine TROKE IS A LEADING cause of long-term disability in S the United States, affecting more than 6.5 million people. The impairment and functional loss induced by stroke are often
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severe in the hand,2-5 reducing independence and diminishing quality of life. The severity of the problem demands that effective hand rehabilitation interventions be developed based on impairment mechanisms. Although one side of the body is largely unaffected by the stroke, many tasks of daily living require bimanual coordination. Restoration of even the ability to stably grip objects with the paretic hand, while the object is manipulated by the contralateral hand (eg, opening a bottle, pulling out dental floss from a container, zipping up a pocket, removing a cap from a pen), would significantly improve the capacity to perform activities of daily living. Unfortunately, stable grip is typically difficult to achieve in persons with severe hand impairment. Successful grip generation requires that forces generated by the digits are properly scaled and directed with respect to the grasped object surface.6-9 After stroke, force scaling is impaired during graspand-lift tasks.10-13 Additionally, grip strength is reduced,14 force fluctuation during tasks is increased,10 and the ability to execute predictive grip force control is diminished.15,16 Recently, we have shown that force misdirection also plays a substantial role in grasp impairment,17 often resulting in the object slipping out of the person’s grasp. Stroke survivors with severe hand impairment tend to produce large shear forces, parallel to the object surface, in relation to the force normal to the object surface (eg, persons with stroke generated a shear force of 5N while generating a maximum pinch force of 12N with the paretic hand, whereas healthy persons generated a shear force of 6N while generating a maximum pinch force of 45N).17 Thus, although the person may possess sufficient strength to grip the object, the improper force direction (ie, high ratio of shear force to normal force) causes the object to
List of Abbreviations ANOVA ARAT BBT EDC FDI FDS IP MANOVA MVC
analysis of variance Action Research Arm Test Box and Block Test extensor digitorum communis first dorsal interosseous flexor digitorum superficialis interphalangeal multivariate analysis of variance maximum voluntary contraction
DIGIT FORCE DIRECTION POSTSTROKE, Seo
slide away from the digits.18 The mean ratio of shear force to normal force at the thumb and the index finger tips during static grip against a fixed object was almost 3 times as great for persons with stroke as for age-matched, neurologically intact persons and the nonparetic digits of the persons with stroke.17 One of the sources for digit force misdirection may be lesions affecting the corticospinal tract resulting in altered muscle activation patterns (ie, diminished excitation of intrinsic muscles and extrinsic extensor muscles, and relatively hyperexcited long finger flexor muscles17,19,20). Such alteration in muscle activation patterns can cause the digit force to be directed close to the distal direction from the fingertip (as opposed to the palmar direction) and, thus, more tangentially than orthogonally relative to the grip surface during pinch grip.8,21-23 Alternatively, impaired perception of sensation caused by lesions affecting somatosensory and motor cortices can contribute to digit force misdirection as described below. Digit force coordination uses tactile feedback from the skin of the finger.6,7,24,25 Reduced sensation and consequent impairment in the closed-loop control26-28 after stroke may contribute to the altered digit force direction (ie, abnormally high shear to normal force ratio). Persons with stroke may not realize that they are producing finger forces with excessive shear force. Salient task-relevant sensory feedback29,30 has shown promise in improving motor recovery after stroke.31-35 For instance, persons with chronic stroke could reduce excessive grip force after training using visual feedback of their actual grip force in relation to a target grip force.31 The objective of this study was to investigate whether visual feedback of digit force directions for the index fingertip and thumb tip during repeated practice of grip force production can correct the digit force directions for persons with stroke during grip assessments. The effect size in the shear to normal force ratio was 17%, which is half of the difference in the force ratio between the paretic hands and asymptomatic hands in the previous study,17 assuming that feedback training only compensates for the sensory impairment, not motor impairment. An instrument to measure and display 3-dimensional digit forces was developed and used in a 4-session training protocol. Force direction and performance of clinical assessments were evaluated before and after completion of the training protocol in persons with chronic hand impairment after stroke. METHODS Study Participants Eleven persons with chronic hemiparesis subsequent to stroke participated in this study. The inclusion criteria were (1) the occurrence of a single stroke at least 9 months before the study; (2) severe hand impairment as indicated by a rating of stage 2 to 3 for the Hand section of the Chedoke-McMaster Stroke Assessment36; and (3) the ability to produce a 5-N pinch force (equivalent to approximately 8% of the mean pinch strength for healthy older adults37) against a fixed instrumented object (fig 1A) with the distal phalanges of the paretic thumb and index finger. Subjects were permitted to pinch through their preferred digit orientation (ie, producing force with either the palmar or lateral aspects of the digits). The exclusion criteria were (1) cognitive dysfunction that precluded comprehension of experimental tasks; and (2) history or clinical signs of concurrent medical problems such as an orthopedic condition in the hand. Time elapsed since stroke ranged from 2 to 20 years. The mean age ⫾ SD was 56⫾9 years (range, 38 – 69y). Eight participants exhibited sensory deficits for the paretic fingertip pads, determined by the 2-point discrimination test (with the
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threshold distance ⱖ6mm).38,39 Three participants did not exhibit sensory deficits for the paretic digits. Nonparetic digits did not demonstrate sensory deficits for any participant. All participants signed the consent form approved by the Institutional Review Board before beginning participation in the study. Procedure To evaluate the effect of training with visual feedback, each subject participated in 4 training sessions, along with 2 evaluation sessions. The 1-hour training sessions were spread over 2 weeks. Evaluation sessions were performed before the first training session and immediately after the last training session. Outcomes were compared between the 2 evaluation sessions (before vs after training) for each study participant. The study participants did not receive additional therapy during the 2 weeks. Training. Participants were seated with the elbow flexed at 90°, the forearm strapped to a horizontal table, and the wrist held in the neutral posture with a splint. The training consisted of controlling forces applied by the paretic thumb and index finger to an instrumented object (see fig 1A). This instrumented object17 consisted of 2 independent plates, each connected to a miniature load cell (Nano17, Mini40).a The load cells measured the 3-dimensional forces applied by the thumb and the index finger separately. The grip surfaces on the plate were covered with a sheet of rubber with a coefficient of friction of 0.9 with respect to the skin40 to minimize finger-object slip. The distal segments of the index finger and thumb were positioned against the plates. During the training, participants strove to control the shear and normal forces applied to the instrumented object with each of the 2 digits. Visual feedback was displayed on a computer screen (fig 1B) with a refresh rate of 0.1Hz. Namely, 2 glasses were shown, each representing each digit force (one for the thumb and the other for the index finger). The magnitude and direction of the shear forces were represented by the location of the bottom of the glass. Thus, the (Fx,Fy) shear forces were mapped to the (x,y) glass location. Zero shear force mapped to the origin in the center of the screen. Normal force was represented as the water level in the glass. Participants were instructed to attempt to position the bottoms of the 2 glasses within the shown target circle, while keeping the water level in the glass (actual normal force) above the tick marks (required normal force) (see fig 1B). The goal was to maintain this magnitude and direction of force for a period of at least 1 second. The software controlling the display was written in MATLAB.b A given trial ended when the participant accomplished the task or when the maximum allowed period of 30 seconds passed, whichever came first. On the completion of a trial, the lowest ratios of absolute shear force error to normal force for each digit were recorded. Shear force error was computed as the norm of the vector from the required (Fx,Fy) shear forces for the glasses to be at the center of the target circle to the actual shear forces. Each training session had a total of 84 trials (14 consecutive trials per block ⫻ 6 blocks per session). A minimum of 3 minutes of rest break was provided between consecutive blocks. The center of the target circle was at the origin for 6 of 14 trials in a block. For the other 8 trials, the center of the target circle was at 1 of the 8 positions surrounding the center circle (see fig 1B). The distance between the origin and the center of each of the 8 surrounding target circles was set equal to 50% of the target normal force. The target normal force was 20% of the normal force recorded during maximum grip during the preArch Phys Med Rehabil Vol 92, January 2011
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DIGIT FORCE DIRECTION POSTSTROKE, Seo
Shear force in the vertical direction
B
(Thumb) (Index finger)
Shear force in the horizontal direction
Actual normal force Required normal force
O (0,0)
Target circles Fig 1. For training and evaluation of the digit force direction, study participants grasped the instrumented object (A) that recorded shear force and normal force at the digit for the thumb and the index finger separately. During training, visual feedback of shear force and normal force was provided to study participants on a computer screen (B). The magnitude and direction of shear force is shown as the location of the glass, and the magnitude of normal force is shown as the height of the water in the glass for each finger. Shear force would move the glasses away from the origin. Study participants were instructed to locate the bottoms of the 2 glasses in a prescribed target circle, while keeping the water level in the glass (actual normal force) above the tick marks (required normal force) as shown in (B). Only one prescribed target circle was shown to the study participants at a time.
A
Shear force in the vertical direction Shear force in the horizontal direction Load cell
training evaluation for each participant. The target normal force ranged from 1.3 to 3.5N depending on the participant’s strength. Initially, the radius of the target circle was 60% of the target normal force. The radius decreased 2% when the participant successfully accomplished more than 80% of the trials in a block. The radius increased 2% when the participant accomplished less than 20% of the trials in a block. Evaluation. For evaluation sessions, digit force direction and clinical hand function scores were measured. Hand motor control was evaluated using the BBT41,42 and the ARAT.43 For digit force direction, participants were instructed to generate 2N, 5N, and maximum pinch force perpendicular to the instrumented object (see fig 1A) using the paretic index finger and thumb. The 3-dimensional forces for each digit were recorded. Visual feedback of normal force magnitude was provided during the 2- and 5-N pinch to enable participants to match the target normal force level. No visual feedback of shear force, however, was provided during the evaluation. Arch Phys Med Rehabil Vol 92, January 2011
Load cell
In addition to the digit forces, electromyographic signals of 4 hand muscles were recorded with surface electrodesc during grip. The targeted muscles were FDS, EDC, FDI, and the thenar eminence (abductor pollicis brevis, flexor pollicis brevis, opponens pollicis muscles). Electromyographic signals were sampled at 500Hz, notch filtered at 60, 120, and 180Hz, rectified, low-pass filtered at 10Hz, and normalized to the MVC. The MVC was obtained before the start of each evaluation while participants maximally contracted each corresponding muscle against resistance. The peak value of the processed electromyographic signals served as the 100% MVC value and was used to normalize electromyographic data. Digit postures were recorded using a camera-based system (OptoTrak3020).d Three infrared markers were placed on the thumb (tip, IP joint, metacarpophalangeal joint), 3 markers on the index finger (fingertip, distal and proximal IP joints), and 3 markers on the object. The “orientation angle” (angle between the digit plane [composed of 3 points of 1 digit] and grip
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DIGIT FORCE DIRECTION POSTSTROKE, Seo
Fig 2. The shear to normal force ratio significantly decreased (A), and the BBT score (B) and the ARAT score (C) significantly increased after the training (*P<.05 for all; mean ⴞ SE).
surface) and “contact angle” (angle between the grip surface and the long axis of the distal phalanx within the digit plane) were computed as in the previous study.17 The index finger orientation angle is normally close to 90° for tip pinch and 0° during lateral pinch. The contact angle is 0° when the distal phalanx is parallel to the grip surface, and 90° when it is orthogonal to the grip surface. After evaluations, the shear to normal force ratio, electromyographic signals, and orientation and contact angles were averaged over the 1-second period during which the mean normal force for the digits was the greatest for maximal pinch or closest to the target normal force for the 2- and 5-N pinch. The shear to normal force ratio was used instead of absolute shear force values, since the interest lies in the digit force direction regardless of normal force levels. Even for 2- and 5-N pinch grips for which visual feedback of actual and target normal force was provided, actual normal force had some deviation from the target normal force. Thus, the shear to normal force ratio was examined for all pinch grip force levels to investigate digit force direction. The “relative electromyographic magnitude” was computed as the ratio of one muscle’s electromyographic magnitude (in %MVC) to the sum of the electromyographic magnitudes (in %MVC) of all 4 muscles measured. The relative electromyographic magnitude for each muscle was computed to examine electromyographic magnitudes for each of the 4 muscles in comparison with one another. An increase in the relative electromyographic magnitude of one muscle could be due to either increased electromyographic activity of the muscle or decreased electromyographic activities of other muscles. Statistical Analysis Repeated measures MANOVA was performed to examine whether the shear to normal force ratio during grip, the BBT score, and the ARAT score significantly varied with training (before, after). Once training was found significant, 3 separate analyses were performed for each measure. Specifically, 2 paired t tests were performed to evaluate the effect of training on the BBT and ARAT scores. Repeated measures ANOVA was performed to determine whether the shear to normal force ratio (measured for the thumb and the index finger separately) significantly changed with training, digit (thumb, index finger), and their interaction. To examine the progress in the force
direction during training, repeated measures ANOVA was performed for the ratio of shear force error to normal force with a within-subject variable of session. After session was found to be significant, post hoc Tukey tests were performed to evaluate differences among the 4 sessions. As secondary analyses, a paired t test was performed to examine whether the study participants’ maximum pinch force changed after training. In addition, repeated measures ANOVA was performed to examine whether the relative electromyographic magnitude changed after training. The within-subject variables of training and muscle (FDS, FDI, EDC, and thenar eminence) and their interaction were tested. Lastly, repeated measures MANOVA was performed to examine whether the orientation angle and contact angle significantly changed after training. RESULTS Digit Force Direction and Hand Function Before Versus After Training After the training protocol, participants were able to direct digit force closer to the direction normal to the object surface during pinch grip. The mean shear to normal force ratio significantly decreased from 58% to 41% (fig 2A). Additionally, scores on the clinical assessments of hand motor control improved. The mean BBT score increased from 1.4 to 3.4 for a gain of 2.0 (SD, 2.0) (fig 2B), and the mean ARAT score (maximum score, 57) increased from 10.8 to 12.1 for a gain of 1.3 (SD, 1.3) (fig 2C). Training was found to be significant (P⬍.05) in the MANOVA, as well as in individual analyses for all 3 measures (P⬍.01 for force ratio and BBT, P⫽.03 for ARAT). The digit (thumb, index finger) and the interaction between digit and training were not significant for the force ratio (P⬎.05). The maximum pinch force for the study participants did not significantly change after training (P⬎.05 from paired t test). Change in Digit Force Direction Across Sessions The ratio of shear force error to normal force was examined across evaluations and training sessions (fig 3). The ratio decreased in the first training session (40%) compared with that obtained in the pretraining evaluation (58%). The mean force Arch Phys Med Rehabil Vol 92, January 2011
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DIGIT FORCE DIRECTION POSTSTROKE, Seo
* * * Shear force error Normal force
60% 30%
With visual feedback
0% pre
1 2 3 4 training sessions
post
Fig 3. The mean ratio of shear force error to normal force before, during the 4 sessions of, and after the training (averaged for all 84 trials for each training session). Visual feedback of shear force was provided only during the training sessions. *The ratio was significantly different between the pre- and post-training evaluations, and between the first training session and the third and fourth training sessions.
ratio further decreased over the subsequent training sessions. The mean ratios in the third and fourth training sessions were lower than that in the first training session (P⬍.01). Muscle Activation Pattern and Digit Posture Before Versus After the Training The mean electromyographic signal magnitude in %MVC was 22%, 23%, 17%, and 18% before training, and 17%, 20%, 16%, and 15% after training for the FDS, EDC, FDI, and thenar eminence, respectively. The mean relative electromyographic magnitudes for the FDS and thenar eminence muscles decreased after training, whereas those for the EDC and FDI muscles increased after training (fig 4). In addition to the main effects of training and muscle (P⬍.01), the interaction between muscle and training was significant (P⫽.04), thereby implying that muscle activation patterns changed after training. The orientation and contact angles did not significantly change with training (P⬎.05). DISCUSSION The results demonstrate that after repeated practice of pinch with visual feedback of force direction, participants with chronic stroke were able to redirect the digit force closer to the direction normal to the object surface during pinch (see fig 2A). This improvement persisted even without visual feedback. Increases in BBT and ARAT hand function scores (142% and 12%, respectively) accompanied the improved force directions (see figs 2B, 2C). Although the changes in the clinical hand function scores were smaller than what have been deemed minimum clinically important differences,44 these statistically significant improvements were achieved after only four 1-hour sessions consisting entirely of isometric pinch tasks. Additionally, the improvements were achieved in persons with severe impairment who may have little chance of motor recovery.45,46 The altered digit force direction (ie, pretraining evaluation mean shear to normal force ratio, 58%) (see fig 2A) may be attributable to both sensory6,7,24,25 and motor deficits.19,20,47 This study attempted to compensate for potentially reduced tactile feedback after stroke by providing immediate visual feedback of digit force direction. This compensation for the sensory deficit may account for the rapid improvement observed in the first training session. Additionally, the training Arch Phys Med Rehabil Vol 92, January 2011
may have provided participants with sensorimotor stimulation48 and repeated practice of motor skills to generate digit forces in the direction they wanted. This motor practice may account for the small but gradual improvement in the force direction in the subsequent training sessions (see fig 3). Review of individual participants’ performance in the pre- and posttraining evaluations revealed that not only those with tactile sensory deficit but also those without tactile sensory deficit, determined by the 2-point discrimination test,38,39 had improvements in the digit force direction and hand function scores. The motor practice may explain improvements seen for participants without tactile sensory deficit. Compensated tactile feedback and sensorimotor stimulation, however, may be insufficient if impairment exists in the corticomotor system. In that case, intervention at the motor system such as neuromuscular electrical stimulation49 may be explored. The improved digit force direction was accompanied by changes in hand muscle activation patterns even while the digit posture (orientation and contact angles) was maintained. Specifically, for the same hand posture, the increased relative electromyographic magnitudes for the EDC and FDI muscles compared with the FDS and thenar eminence after the training (see fig 4) may have helped improve the digit force direction. The extensor and intrinsic muscles of the hand play an important role in controlling the digit force direction, and the activities of the extensor and intrinsic muscles are often greater than that of the FDS muscle during grip in neurologically intact persons.8,17,22,50,51 Suppression of EDC and FDI muscle activity and hyperexcitability of the FDS muscle after stroke could disturb proper motor control of the hand and fingers,19,20,47,52 and contribute to the altered digit force direction in the paretic hand.17,21 This study shows that participants with chronic stroke could modify their hand muscle activation patterns for grip toward the pattern observed in neurologically intact persons through training using feedback. This is consistent with the previous study demonstrating the modifiability in the arm muscle activation pattern in the chronic stroke population via training using visual feedback.32 Study Limitations Learning could have played a role in enhancing the BBT and ARAT scores for the evaluation sessions before and after training, although the tasks in BBT and ARAT are functional movements that may not require much familiarization. Future studies, including a control group performing the training without visual feedback, are warranted to assess the effects of extended feedback training on hand motor control and the extent to which any associated improvements are maintained.
Fig 4. Changes in the relative electromyographic magnitude before and after the training for 4 hand muscles (FDS, EDC, FDI, thenar eminence [Thenar]). The electromyographic signals during pinch grip were rectified and normalized to the electromyographic level during the MVC for each muscle. Then, the ratio of the normalized electromyographic magnitude of each muscle to the sum of the normalized electromyographic magnitude for the 4 muscles was computed. The change in this ratio with training (the ratio after the training minus the ratio before the training) and its SE for each muscle are shown in the figure (grip force level pooled).
DIGIT FORCE DIRECTION POSTSTROKE, Seo
CONCLUSIONS Repeated practice of pinch was performed with visual feedback provided through an interactive training tool. After 4 training sessions, stroke survivors with severe hand impairment showed substantial improvement in the ability to direct digit forces toward a grasped object. Changes in muscle activation patterns accompanied the improvement in force direction, as did improved performance on clinical assessments of hand function (BBT and ARAT). Use of this training paradigm in conjunction with other therapies may help improve hand function among persons with chronic stroke. References 1. Lloyd-Jones D, Adams R, Carnethon M, et al. Heart disease and stroke statistics—2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2009;119:480-6. 2. Gray CS, French JM, Bates D, Cartlidge NE, James OF, Venables G. Motor recovery following acute stroke. Age Ageing 1990;19: 179-84. 3. Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS. Recovery of upper extremity function in stroke patients: the Copenhagen Stroke Study. Arch Phys Med Rehabil 1994;75:394-8. 4. Parker VM, Wade DT, Langton Hewer R. Loss of arm function after stroke: measurement, frequency, and recovery. Int Rehabil Med 1986;8:69-73. 5. Woodson AM. Stroke. In: Trombly CA, editor. Occupational therapy for physical dysfunction. Philadelphia: Lippincott, Williams & Wilkins; 2002. p 817-53. 6. Johansson RS, Westling G. Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects. Exp Brain Res 1984;56: 550-64. 7. Gordon AM, Forssberg H, Johansson RS, Westling G. Integration of sensory information during the programming of precision grip: comments on the contributions of size cues. Exp Brain Res 1991; 85:226-9. 8. Johanson ME, Valero-Cuevas FJ, Hentz VR. Activation patterns of the thumb muscles during stable and unstable pinch tasks. J Hand Surg [Am] 2001;26:698-705. 9. Latash ML, Zatsiorsky VM. Multi-finger prehension: control of a redundant mechanical system. Adv Exp Med Biol 2009;629:597618. 10. Blennerhassett JM, Carey LM, Matyas TA. Grip force regulation during pinch grip lifts under somatosensory guidance: comparison between people with stroke and healthy controls. Arch Phys Med Rehabil 2006;87:418-29. 11. Blennerhassett JM, Carey LM, Matyas TA. Clinical measures of handgrip limitation relate to impaired pinch grip force control after stroke. J Hand Ther 2008;21:245-52; quiz 53. 12. McDonnell MN, Hillier SL, Ridding MC, Miles TS. Impairments in precision grip correlate with functional measures in adult hemiplegia. Clin Neurophysiol 2006;117:1474-80. 13. Nowak DA, Grefkes C, Dafotakis M, Kust J, Karbe H, Fink GR. Dexterity is impaired at both hands following unilateral subcortical middle cerebral artery stroke. Eur J Neurosci 2007; 25:3173-84. 14. Boissy P, Bourbonnais D, Carlotti MM, Gravel D, Arsenault BA. Maximal grip force in chronic stroke subjects and its relationship to global upper extremity function. Clin Rehabil 1999;13:354-62. 15. Nowak DA, Hermsdorfer J, Topka H. Deficits of predictive grip force control during object manipulation in acute stroke. J Neurol 2003;250:850-60. 16. Nowak DA, Hermsdorfer J. Grip force behavior during object manipulation in neurological disorders: toward an objective
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38. Magee DJ. Orthopedic physical assessment. St Louis: Saunders; 2007. 39. Novak CB, Mackinnon SE, Kelly L. Correlation of two-point discrimination and hand function following median nerve injury. Ann Plast Surg 1993;31:495-8. 40. Seo NJ, Armstrong TJ. Friction coefficients in a longitudinal direction between the finger pad and selected materials for different normal forces and curvatures. Ergonomics 2009;52:609-16. 41. Mathiowetz V, Volland G, Kashman N, Weber K. Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther 1985;39:386-91. 42. Desrosiers J, Bravo G, Hebert R, Dutil E, Mercier L. Validation of the Box and Block Test as a measure of dexterity of elderly people: reliability, validity, and norms studies. Arch Phys Med Rehabil 1994;75:751-5. 43. Lang CE, Wagner JM, Dromerick AW, Edwards DF. Measurement of upper-extremity function early after stroke: properties of the Action Research Arm Test. Arch Phys Med Rehabil 2006;87: 1605-10. 44. Van der Lee JH, De Groot V, Beckerman H, Wagenaar RC, Lankhorst GJ, Bouter LM. The intra- and interrater reliability of the Action Research Arm Test: a practical test of upper extremity function in patients with stroke. Arch Phys Med Rehabil 2001; 82:14-9. 45. Hendricks HT, van Limbeek J, Geurts AC, Zwarts MJ. Motor recovery after stroke: a systematic review of the literature. Arch Phys Med Rehabil 2002;83:1629-37. 46. Binkofski F, Seitz RJ, Hacklander T, Pawelec D, Mau J, Freund HJ. Recovery of motor functions following hemiparetic stroke: a
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