Finger strength, individuation, and their interaction: Relationship to hand function and corticospinal tract injury after stroke

OBJECTIVE The goal of this study was to determine the relative contributions of finger weakness and reduced finger individuation to reduced hand function after stroke, and their association with corticospinal tract (CST) injury. METHODS We measured individuated and synergistic maximum voluntary contractions (MVCs) of the index and middle fingers, in both flexion and extension, of 26 individuals with a chronic stroke using a robotic exoskeleton. We quantified finger strength and individuation, and defined a novel metric that combines them - "multifinger capacity". We used stepwise linear regression to identify which measure best predicted hand function (Box and Blocks Test, Nine Hole Peg Test) and arm impairment (the Upper Extremity Fugl-Meyer Test). RESULTS Compared to metrics of strength or individuation, capacity survived the stepwise regression as the strongest predictor of hand function and arm impairment. Capacity was also most strongly related to presence or absence of lesion overlap with the CST. CONCLUSIONS Reduced strength and individuation combine to shrink the space of achievable finger torques, and it is the resulting size of this space - the multifinger capacity - that is of elevated importance for predicting loss of hand function. SIGNIFICANCE Multi-finger capacity may be an important target for rehabilitative hand training.

[1]  M. Latash,et al.  The effects of stroke and age on finger interaction in multi-finger force production tasks , 2003, Clinical Neurophysiology.

[2]  Andrea N. Reinkensmeyer,et al.  Retraining and assessing hand movement after stroke using the MusicGlove: comparison with conventional hand therapy and isometric grip training , 2014, Journal of NeuroEngineering and Rehabilitation.

[3]  Derek G. Kamper,et al.  Impairment in Task-Specific Modulation of Muscle Coordination Correlates with the Severity of Hand Impairment following Stroke , 2013, PloS one.

[4]  L. Ada,et al.  Loss of strength contributes more to physical disability after stroke than loss of dexterity , 2004, Clinical rehabilitation.

[5]  Steven C Cramer,et al.  Anatomy of Stroke Injury Predicts Gains From Therapy , 2011, Stroke.

[6]  Marc H Schieber,et al.  Selective activation of human finger muscles after stroke or amputation. , 2009, Advances in experimental medicine and biology.

[7]  Cathy C. Y. Chou,et al.  A Standardized Approach to the Fugl-Meyer Assessment and Its Implications for Clinical Trials , 2013, Neurorehabilitation and neural repair.

[8]  Babak Shahbaba,et al.  Neural function, injury, and stroke subtype predict treatment gains after stroke , 2015, Annals of neurology.

[9]  Preeti Raghavan,et al.  Patterns of impairment in digit independence after subcortical stroke. , 2006, Journal of neurophysiology.

[10]  Thierry Keller,et al.  Neck rotation modulates flexion synergy torques, indicating an ipsilateral reticulospinal source for impairment in stroke. , 2012, Journal of neurophysiology.

[11]  Vicky Chan,et al.  Robotic Assistance for Training Finger Movement Using a Hebbian Model: A Randomized Controlled Trial , 2017, Neurorehabilitation and neural repair.

[12]  Marc A. Maier,et al.  A novel method for the quantification of key components of manual dexterity after stroke , 2015, Journal of NeuroEngineering and Rehabilitation.

[13]  H. Noda,et al.  Recovery of voluntary movement in hemiplegic patients. Correlation with degenerative shrinkage of the cerebral peduncles in CT images. , 1990, Brain : a journal of neurology.

[14]  Qinyin Qiu,et al.  Journal of Neuroengineering and Rehabilitation Design of a Complex Virtual Reality Simulation to Train Finger Motion for Persons with Hemiparesis: a Proof of Concept Study , 2022 .

[15]  Catherine E Lang,et al.  Relating Movement Control at 9 Upper Extremity Segments to Loss of Hand Function in People with Chronic Hemiparesis , 2007, Neurorehabilitation and neural repair.

[16]  G. Schlaug,et al.  Structural integrity of corticospinal motor fibers predicts motor impairment in chronic stroke , 2010, Neurology.

[17]  A. Sunderland,et al.  Arm function after stroke: measurement and recovery over the first three months. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[18]  V. Mathiowetz,et al.  Adult norms for the Box and Block Test of manual dexterity. , 1985, The American journal of occupational therapy : official publication of the American Occupational Therapy Association.

[19]  R W Bohannon,et al.  Motor variables correlated with the hand-to-mouth maneuver in stroke patients. , 1991, Archives of physical medicine and rehabilitation.

[20]  M. Schieber,et al.  Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. , 2003, Journal of neurophysiology.

[21]  A. Sterr,et al.  The Role of Corticospinal Tract Damage in Chronic Motor Recovery and Neurorehabilitation: A Pilot Study , 2010, Neurorehabilitation and neural repair.

[22]  Justin B. Rowe,et al.  Design and preliminary evaluation of the FINGER rehabilitation robot: controlling challenge and quantifying finger individuation during musical computer game play , 2014, Journal of NeuroEngineering and Rehabilitation.

[23]  Derek G Kamper,et al.  Training finger individuation with a mechatronic-virtual reality system leads to improved fine motor control post-stroke , 2014, Journal of NeuroEngineering and Rehabilitation.

[24]  H. Benali,et al.  Contribution of Corticospinal Tract and Functional Connectivity in Hand Motor Impairment after Stroke , 2013, PloS one.

[25]  Derek G. Kamper,et al.  Isokinetic strength and power deficits in the hand following stroke , 2012, Clinical Neurophysiology.

[26]  Dae-Shik Kim,et al.  Motor outcome according to the integrity of the corticospinal tract determined by diffusion tensor tractography in the early stage of corona radiata infarct , 2007, Neuroscience Letters.

[27]  Derek G Kamper,et al.  Investigation of hand muscle atrophy in stroke survivors. , 2012, Clinical biomechanics.

[28]  M. Schieber,et al.  Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. , 2004, Journal of neurophysiology.

[29]  E. G. Cruz,et al.  Weakness is the primary contributor to finger impairment in chronic stroke. , 2006, Archives of physical medicine and rehabilitation.

[30]  Joseph D. Towles,et al.  Finger-thumb coupling contributes to exaggerated thumb flexion in stroke survivors. , 2014, Journal of neurophysiology.

[31]  Agnès Roby-Brami,et al.  Affected and unaffected quantitative aspects of grip force control in hemiparetic patients after stroke , 2012, Brain Research.

[32]  Gary W. Thickbroom,et al.  Motor outcome after subcortical stroke: MEPs correlate with hand strength but not dexterity , 2002, Clinical Neurophysiology.

[33]  Jörn Diedrichsen,et al.  Separable systems for recovery of finger strength and control after stroke. , 2017, Journal of neurophysiology.

[34]  BumChul Yoon,et al.  The effect of stroke on motor selectivity for force control in single- and multi-finger force production tasks. , 2014, NeuroRehabilitation.

[35]  B. Brouwer,et al.  Hand function and motor cortical output poststroke: are they related? , 2006, Archives of physical medicine and rehabilitation.

[36]  Julius P. A. Dewald,et al.  Robotic quantification of upper extremity loss of independent joint control or flexion synergy in individuals with hemiparetic stroke: a review of paradigms addressing the effects of shoulder abduction loading , 2016, Journal of NeuroEngineering and Rehabilitation.

[37]  John W. Krakauer,et al.  Motor control of the hand before and after stroke , 2015 .

[38]  Sung Ho Jang,et al.  The role of the corticospinal tract in motor recovery in patients with a stroke: a review. , 2009, NeuroRehabilitation.

[39]  S. C. Gandevia,et al.  Strength Changes in Hemiparesis: Measurements and Mechanisms , 1993 .

[40]  W. Rymer,et al.  Relative contributions of neural mechanisms versus muscle mechanics in promoting finger extension deficits following stroke , 2003, Muscle & nerve.

[41]  Jeffrey D. Riley,et al.  A multimodal approach to understanding motor impairment and disability after stroke , 2014, Journal of Neurology.

[42]  Steven C Cramer,et al.  Anatomy and physiology predict response to motor cortex stimulation after stroke , 2011, Neurology.

[43]  Adriana Bastos Conforto,et al.  Corticospinal Tract Integrity and Lesion Volume Play Different Roles in Chronic Hemiparesis and Its Improvement Through Motor Practice , 2014, Neurorehabilitation and neural repair.

[44]  Etienne Burdet,et al.  A technique to train finger coordination and independence after stroke , 2010, Disability and rehabilitation. Assistive technology.

[45]  P M Matthews,et al.  Relating MRI changes to motor deficit after ischemic stroke by segmentation of functional motor pathways. , 2000, Stroke.

[46]  M H Schieber,et al.  Partial Inactivation of the Primary Motor Cortex Hand Area: Effects on Individuated Finger Movements , 1998, The Journal of Neuroscience.

[47]  M. Schieber.  Individuated finger movements of rhesus monkeys: a means of quantifying the independence of the digits. , 1991, Journal of neurophysiology.

[48]  Vicky Chan,et al.  Robot-assisted Guitar Hero for finger rehabilitation after stroke , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[49]  Robert Lindenberg,et al.  Lesion Load of the Corticospinal Tract Predicts Motor Impairment in Chronic Stroke , 2010, Stroke.

[50]  Janice J Eng,et al.  Paretic Upper-Limb Strength Best Explains Arm Activity in People With Stroke , 2007, Physical Therapy.

[51]  W. Rymer,et al.  Impairment of voluntary control of finger motion following stroke: Role of inappropriate muscle coactivation , 2001, Muscle & nerve.

[52]  L. Chan,et al.  Incidence, prevalence, costs, and impact on disability of common conditions requiring rehabilitation in the United States: stroke, spinal cord injury, traumatic brain injury, multiple sclerosis, osteoarthritis, rheumatoid arthritis, limb loss, and back pain. , 2014, Archives of physical medicine and rehabilitation.