Dynamical Coordination of Hand Intrinsic Muscles for Precision Grip in Diabetes Mellitus

This study investigated the effects of diabetes mellitus (DM) on dynamical coordination of hand intrinsic muscles during precision grip. Precision grip was tested using a custom designed apparatus with stable and unstable loads, during which the surface electromyographic (sEMG) signals of the abductor pollicis brevis (APB) and first dorsal interosseous (FDI) were recorded simultaneously. Recurrence quantification analysis (RQA) was applied to quantify the dynamical structure of sEMG signals of the APB and FDI; and cross recurrence quantification analysis (CRQA) was used to assess the intermuscular coupling between the two intrinsic muscles. This study revealed that the DM altered the dynamical structure of muscle activation for the FDI and the dynamical intermuscular coordination between the APB and FDI during precision grip. A reinforced feedforward mechanism that compensates the loss of sensory feedbacks in DM may be responsible for the stronger intermuscular coupling between the APB and FDI muscles. Sensory deficits in DM remarkably decreased the capacity of online motor adjustment based on sensory feedback, rendering a lower adaptability to the uncertainty of environment. This study shed light on inherent dynamical properties underlying the intrinsic muscle activation and intermuscular coordination for precision grip and the effects of DM on hand sensorimotor function.

[1]  J. Napier,et al.  The attachments and function of the abductor pollicis brevis. , 1952, Journal of anatomy.

[2]  J. F. Soechting,et al.  Sensorimotor control of contact force , 2008, Current Opinion in Neurobiology.

[3]  S. Gorniak,et al.  Detecting subtle fingertip sensory and motor dysfunction in adults with type II diabetes , 2014, Experimental Brain Research.

[4]  F. Su,et al.  How the Impact of Median Neuropathy on Sensorimotor Control Capability of Hands for Diabetes: An Achievable Assessment from Functional Perspectives , 2014, PloS one.

[5]  Karen L Price,et al.  Development and validity testing of the neuropathy total symptom score-6: questionnaire for the study of sensory symptoms of diabetic peripheral neuropathy. , 2005, Clinical therapeutics.

[6]  M. Hepp-Reymond,et al.  EMG activation patterns during force production in precision grip , 2004, Experimental Brain Research.

[7]  Peter J. Evans,et al.  Carpal tunnel syndrome impairs sustained precision pinch performance , 2015, Clinical Neurophysiology.

[8]  M. Santello,et al.  Common input to motor units of intrinsic and extrinsic hand muscles during two-digit object hold. , 2008, Journal of neurophysiology.

[9]  Tomoyoshi Komiyama,et al.  Location-specific and task-dependent modulation of cutaneous reflexes in intrinsic human hand muscles , 2006, Clinical Neurophysiology.

[10]  Na Wei,et al.  Effects of Tactile Sensitivity on Structural Variability of Digit Forces during Stable Precision Grip , 2016, BioMed research international.

[11]  S. Gorniak,et al.  Changes in sensory function and force production in adults with type II diabetes , 2014, Muscle & nerve.

[12]  E. Maltezos,et al.  The diabetic hand: a forgotten complication? , 2010, Journal of diabetes and its complications.

[13]  Marco Santello,et al.  Force-independent distribution of correlated neural inputs to hand muscles during three-digit grasping. , 2010, Journal of neurophysiology.

[14]  Eva L Feldman,et al.  Diabetic neuropathy: clinical manifestations and current treatments , 2012, The Lancet Neurology.

[15]  J. Bell-Krotoski,et al.  The repeatability of testing with Semmes-Weinstein monofilaments. , 1987, The Journal of hand surgery.

[16]  D. Cocito,et al.  Electrodiagnostic testing in diabetic neuropathy: Which limb? , 2015, Diabetes Research and Clinical Practice.

[17]  A. Vinik,et al.  Painful diabetic peripheral neuropathy: consensus recommendations on diagnosis, assessment and management , 2011, Diabetes/metabolism research and reviews.

[18]  C. Cooper,et al.  Type 2 diabetes, muscle strength, and impaired physical function: the tip of the iceberg? , 2005, Diabetes care.

[19]  K. Eriksson,et al.  Hand disorders, hand function, and activities of daily living in elderly men with type 2 diabetes. , 2009, Journal of diabetes and its complications.

[20]  A. Weiss,et al.  Hand manifestations of diabetes mellitus. , 2008, The Journal of hand surgery.

[21]  Jürgen Kurths,et al.  Recurrence plots for the analysis of complex systems , 2009 .

[22]  F. Hamdan,et al.  Diabetic hand syndromes as a clinical and diagnostic tool for diabetes mellitus patients. , 2011, Diabetes research and clinical practice.

[23]  Christopher M Laine,et al.  Intermuscular coherence reflects functional coordination. , 2017, Journal of neurophysiology.

[24]  L. Laslett,et al.  Deteriorating tactile sensation in patients with hand syndromes associated with diabetes: a two-year observational study. , 2012, Journal of diabetes and its complications.

[25]  John V. Basmajian,et al.  Electrode placement in EMG biofeedback , 1980 .

[26]  S. Savaş,et al.  The effects of the diabetes related soft tissue hand lesions and the reduced hand strength on functional disability of hand in type 2 diabetic patients. , 2007, Diabetes research and clinical practice.

[27]  C. Rice,et al.  Length dependent loss of motor axons and altered motor unit properties in human diabetic polyneuropathy , 2014, Clinical Neurophysiology.

[28]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Biology.

[29]  R. S. Johansson,et al.  Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects , 2004, Experimental Brain Research.

[30]  Benoni B. Edin,et al.  Coordination of fingertip forces during human manipulation can emerge from independent neural networks controlling each engaged digit , 1997, Experimental Brain Research.

[31]  A. Vinik,et al.  Focal entrapment neuropathies in diabetes. , 2004, Diabetes care.

[32]  J. Nielsen,et al.  Changes in corticospinal drive to spinal motoneurones following tablet‐based practice of manual dexterity , 2016, Physiological reports.

[33]  M. Caccia,et al.  Prevalence of subclinical neuropathy in diabetic patients: assessment by study of conduction velocity distribution within motor and sensory nerve fibres , 1998, Journal of Neurology.

[34]  D. F. Stegeman,et al.  Selective spatial information from surface EMG after temporal filtering: the application to interference EMG using cross-covariance analysis , 2003, Clinical Neurophysiology.

[35]  Michael A Nordstrom,et al.  A comparison of cross-correlation and surface EMG techniques used to quantify motor unit synchronization in humans , 1999, Journal of Neuroscience Methods.

[36]  Dominic Thewlis,et al.  Coordination of digit force variability during dominant and non-dominant sustained precision pinch , 2015, Experimental Brain Research.

[37]  Veronica J Santos,et al.  Precision grip responses to unexpected rotational perturbations scale with axis of rotation. , 2013, Journal of biomechanics.

[38]  Mehmet Akif Buyukbese,et al.  Hand grip strength in patients with type 2 diabetes mellitus. , 2005, Diabetes research and clinical practice.

[39]  C L Webber,et al.  Dynamical assessment of physiological systems and states using recurrence plot strategies. , 1994, Journal of applied physiology.

[40]  Cristian F Pasluosta,et al.  Influence of nerve supply on hand electromyography coherence during a three-digit task. , 2013, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[41]  William V. Massey,et al.  Coherence between surface electromyograms is influenced by electrode placement in hand muscles , 2011, Journal of Neuroscience Methods.

[42]  K. C. A. Lima,et al.  Grip force control during simple manipulation tasks in non-neuropathic diabetic individuals , 2013, Clinical Neurophysiology.

[43]  Ke Li,et al.  Cross recurrence quantification analysis of precision grip following peripheral median nerve block , 2013, Journal of NeuroEngineering and Rehabilitation.

[44]  T. Le,et al.  Epidemiology, public health burden, and treatment of diabetic peripheral neuropathic pain: a review. , 2007, Pain medicine.

[45]  Michael A. Riley,et al.  Dynamical structure of hand trajectories during pole balancing , 2009, Neuroscience Letters.

[46]  A. Boulton,et al.  Diabetic neuropathies and pain. , 1986, Clinics in endocrinology and metabolism.

[47]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[48]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[49]  Zong-Ming Li,et al.  Effects of Carpal Tunnel Syndrome on Force Coordination and Muscle Coherence during Precision Pinch , 2017, Journal of medical and biological engineering.

[50]  Marco Santello,et al.  Neural control of hand muscles during prehension. , 2009, Advances in experimental medicine and biology.

[51]  L. Laslett,et al.  Hand Syndromes Associated with Diabetes: Impairments and Obesity Predict Disability , 2009, The Journal of Rheumatology.

[52]  Mehtap Ozdirenç,et al.  Evaluation of physical fitness in patients with Type 2 diabetes mellitus. , 2003, Diabetes research and clinical practice.

[53]  G. Said,et al.  Diabetic neuropathy—a review , 2007, Nature Clinical Practice Neurology.

[54]  Gabriel Baud-Bovy,et al.  Neural bases of hand synergies , 2013, Front. Comput. Neurosci..

[55]  V. Mathiowetz,et al.  Grip and pinch strength: normative data for adults. , 1985, Archives of physical medicine and rehabilitation.