Priming for Improved Hand Strength in Persons with Chronic Tetraplegia: A Comparison of Priming-Augmented Functional Task Practice, Priming Alone, and Conventional Exercise Training

Joyce Gomes-Osman, Jacqueline A Tibbett, Brandon P Poe, Edelle C Field-Fote, Joyce Gomes-Osman, Jacqueline A Tibbett, Brandon P Poe, Edelle C Field-Fote

Abstract

Many everyday tasks cannot be accomplished without adequate grip strength, and corticomotor drive to the spinal motoneurons is a key determinant of grip strength. In persons with tetraplegia, damage to spinal pathways limits transmission of signals from motor cortex to spinal motoneurons. Corticomotor priming, which increases descending drive, should increase corticospinal transmission through the remaining spinal pathways resulting in increased grip strength. Since the motor and somatosensory cortices share reciprocal connections, corticomotor priming may also have potential to influence somatosensory function. The purpose of this study was to assess changes in grip (precision, power) force and tactile sensation associated with two different corticomotor priming approaches and a conventional training approach and to determine whether baseline values can predict responsiveness to training. Participants with chronic (≥1 year) tetraplegia (n = 49) were randomized to one of two corticomotor priming approaches: functional task practice plus peripheral nerve somatosensory stimulation (FTP + PNSS) or PNSS alone, or to conventional exercise training (CET). To assess whether baseline corticospinal excitability (CSE) is predictive of responsiveness to training, in a subset of participants, we assessed pre-intervention CSE of the thenar muscles. Participants were trained 2 h daily, 5 days/week for 4 weeks. Thirty-seven participants completed the study. Following intervention, significant improvements in precision grip force were observed in both the stronger and weaker hand in the FTP + PNSS group (effect size: 0.51, p = 0.04 and 0.54, p = 0.03, respectively), and significant improvements in weak hand precision grip force were associated with both PNSS and CET (effect size: 0.54, p = 0.03 and 0.75, p = 0.02, respectively). No significant changes were observed in power grip force or somatosensory scores in any group. Across all groups, responsiveness to training as measured by change in weak hand power grip force was correlated with baseline force. Change in precision grip strength was correlated with measures of baseline CSE. These findings indicate that corticomotor priming with FTP + PNSS had the greatest influence on precision grip strength in both the stronger and weaker hand; however, both PNSS and CET were associated with improved precision grip strength in the weaker hand. Responsiveness to training may be associated with baseline CSE.

Keywords: activities of daily living; hand function; human movement system; rehabilitation; spinal cord injury.

Figures

Figure 1
Figure 1
Sample bimanual functional task practice activities. Participants engaged in each category of activity for at least 20 min. The therapist provided verbal or tactile cues as needed to limit the use of compensatory strategies.
Figure 2
Figure 2
Effect sizes for outcomes related to precision vs. power grip. In the weak hand, the standardized response mean met the criterion of 0.5 effect size indicating meaningful change for Pinch (precision grip) and Grasp (power grip) for all three interventions. In the strong hand, the 0.5 criterion were met only in the FTP + PNSS group.
Figure 3
Figure 3
Responsiveness as a function of baseline sensory scores. Top row: change in Pinch [precision grip (A)], Grasp [power grip (B)], and Sensory function (C) in the weak hand as a function of baseline sensory scores of the weak hand. Bottom row: change in Pinch [precision grip (D)], Grasp [power grip (E)], and Sensory function (F) in the strong hand as a function of baseline sensory scores of the strong hand. Key (symbol, line): □ | = functional task practice plus peripheral nerve somatosensory stimulation (FTP + PNSS); ○ ⋮ = PNSS; Δ ¦ = conventional exercise training (CET). Pearson r-values were significant only for the relationship between baseline sensory scores and change in sensory function [Panel (C)] for both the PNSS (r = −0.624, p = 0.011) and CET group (r = −0.695, p = 0.013).

References

    1. National Spinal Cord Injury Statistical Center (NSCISC). Spinal Cord Injury Facts and Figures at a Glance [Internet]. (2016). Available from:
    1. Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma (2004) 21(10):1371–83.10.1089/neu.2004.21.1371
    1. Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-Sorensen F. Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics. Spinal Cord (2004) 42:526–32.10.1038/sj.sc.3101638
    1. Lo C, Tran Y, Anderson K, Craig A, Middleton J. Functional priorities in persons with spinal cord injury: using discrete choice experiments to determine preferences. J Neurotrauma (2016) 33(21):1958–68.10.1089/neu.2016.4423
    1. Zbogar D, Eng JJ, Miller WC, Krassioukov AV, Verrier MC. Movement repetitions in physical and occupational therapy during spinal cord injury rehabilitation. Spinal Cord (2016). Available from:
    1. Smaby N, Johanson ME, Baker B, Kenney DE, Murray WM, Hentz VR. Identification of key pinch forces required to complete functional tasks. J Rehabil Res Dev (2004) 41(2):215–24.10.1682/JRRD.2004.02.0215
    1. Clark BC, Mahato NK, Nakazawa M, Law TD, Thomas JS. The power of the mind: the cortex as a critical determinant of muscle strength/weakness. J Neurophysiol (2014) 112(12):3219–26.10.1152/jn.00386.2014
    1. Darian-Smith I, Galea MP, Darian-Smith C. Manual dexterity: how does the cerebral cortex contribute? Clin Exp Pharmacol Physiol (1996) 23(10–11):948–56.10.1111/j.1440-1681.1996.tb01147.x
    1. Bunday KL, Tazoe T, Rothwell JC, Perez MA. Subcortical control of precision grip after human spinal cord injury. J Neurosci (2014) 34(21):7341–50.10.1523/JNEUROSCI.0390-14.2014
    1. Zagha E, Casale AE, Sachdev RN, McGinley MJ, McCormick DA. Motor cortex feedback influences sensory processing by modulating network state. Neuron (2013) 79(3):567–78.10.1016/j.neuron.2013.06.008
    1. Haider B, McCormick DA. Rapid neocortical dynamics: cellular and network mechanisms. Neuron (2009) 62(2):171–89.10.1016/j.neuron.2009.04.008
    1. Beekhuizen KS, Field-Fote EC. Sensory stimulation augments the effects of massed practice training in persons with tetraplegia. Arch Phys Med Rehabil (2008) 89(4):602–8.10.1016/j.apmr.2007.11.021
    1. Stoykov ME, Madhavan S. Motor priming in neurorehabilitation. J Neurol Phys Ther (2015) 39(1):33–42.10.1097/NPT.0000000000000065
    1. Beekhuizen KS, Field-Fote EC. Massed practice versus massed practice with stimulation: effects on upper extremity function and cortical plasticity in individuals with incomplete cervical spinal cord injury. Neurorehabil Neural Repair (2005) 19:33–45.10.1177/1545968305274517
    1. Hoffman L, Field-Fote E. Effects of practice combined with somatosensory or motor stimulation on hand function in persons with spinal cord injury. Top Spinal Cord Inj Rehabil (2013) 19:288–99.10.1310/sci1904-288
    1. Hoffman LR, Field-Fote EC. Bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys Ther (2007) 87(2):208–23.10.2522/ptj.20050365
    1. Hoffman LR, Field-Fote EC. Functional and corticomotor changes in individuals with tetraplegia following unimanual or bimanual massed practice training with somatosensory stimulation: a pilot study. J Neurol Phys Ther (2010) 34:193–201.10.1097/NPT.0b013e3181fbe692
    1. Gomes-Osman J, Field-Fote EC. Improvements in hand function in adults with chronic tetraplegia following a multiday 10-Hz repetitive transcranial magnetic stimulation intervention combined with repetitive task practice. J Neurol Phys Ther (2015) 39:23–30.10.1097/NPT.0000000000000062
    1. Gomes-Osman J, Field-Fote EC. Cortical vs. afferent stimulation as an adjunct to functional task practice training: a randomized, comparative pilot study in people with cervical spinal cord injury. Clin Rehabil (2015) 29:771–82.10.1177/0269215514556087
    1. Bunday KL, Perez MA. Motor recovery after spinal cord injury enhanced by strengthening corticospinal synaptic transmission. Curr Biol (2012) 22(24):2355–61.10.1016/j.cub.2012.10.046
    1. Kuppuswamy A, Balasubramaniam AV, Maksimovic R, Mathias CJ, Gall A, Craggs MD, et al. Action of 5Hz repetitive transcranial magnetic stimulation on sensory, motor and autonomic function in human spinal cord injury. Clin Neurophysiol (2011) 122(12):2452–61.10.1016/j.clinph.2011.04.022
    1. Belci M, Catley M, Husain M, Frankel HL, Davey NJ. Magnetic brain stimulation can improve clinical outcome in incomplete spinal cord injured patients. Spinal Cord (2004) 42(7):417–9.10.1038/sj.sc.3101613
    1. Yozbatiran N, Keser Z, Davis M, Stampas A, O’Malley MK, Cooper-Hay C, et al. Transcranial direct current stimulation (tDCS) of the primary motor cortex and robot-assisted arm training in chronic incomplete cervical spinal cord injury: a proof of concept sham-randomized clinical study. NeuroRehabilitation (2016) 39(3):401–11.10.3233/NRE-161371
    1. Murray LM, Edwards DJ, Ruffini G, Labar D, Stampas A, Pascual-Leone A, et al. Intensity dependent effects of transcranial direct current stimulation on corticospinal excitability in chronic spinal cord injury. Arch Phys Med Rehabil (2015) 96(4):S114–21.10.1016/j.apmr.2014.11.004
    1. Perez MA, Lungholt BK, Nyborg K, Nielsen JB. Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res (2004) 159(2):197–205.10.1007/s00221-004-1947-5
    1. Leung M, Rantalainen T, Teo WP, Kidgell D. Motor cortex excitability is not differentially modulated following skill and strength training. Neuroscience (2015) 305:99–108.10.1016/j.neuroscience.2015.08.007
    1. Perez MA, Cohen LG. Mechanisms underlying functional changes in the primary motor cortex ipsilateral to an active hand. J Neurosci (2008) 28(22):5631–40.10.1523/JNEUROSCI.0093-08.2008
    1. Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res (2000) 131:135–43.10.1007/s002219900269
    1. Charlton CS, Ridding MC, Thompson PD, Miles TS. Prolonged peripheral nerve stimulation induces persistent changes in excitability of human motor cortex. J Neurol Sci (2003) 208(1–2):79–85.10.1016/S0022-510X(02)00443-4
    1. Zarzecki P, Shinoda Y, Asanuma H. Projection from area 3a to the motor cortex by neurons activated from group I muscle afferents. Exp Brain Res (1978) 33:269–82.10.1007/BF00238065
    1. Kidgell DJ, Frazer AK, Daly RM, Rantalainen T, Ruotsalainen I, Ahtiainen J, et al. Increased cross-education of muscle strength and reduced corticospinal inhibition following eccentric strength training. Neuroscience (2015) 300:566–75.10.1016/j.neuroscience.2015.05.057
    1. Selvanayagam VS, Riek S, Carroll TJ. Early neural responses to strength training. J Appl Physiol (2011) 111(2):367–75.10.1152/japplphysiol.00064.2011
    1. Jensen JL, Marstrand PC, Nielsen JB. Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol (2005) 99(4):1558–68.10.1152/japplphysiol.01408.2004
    1. Latella C, Hendy AM, Pearce AJ, VanderWesthuizen D, Teo W-P. The time-course of acute changes in corticospinal excitability, intra-cortical inhibition and facilitation following a single-session heavy strength training of the biceps brachii. Front Hum Neurosci (2016) 10:607.10.3389/fnhum.2016.00607
    1. Hicks AL, Martin KA, Ditor DS, Latimer AE, Craven C, Bugaresti J, et al. Long-term exercise training in persons with spinal cord injury: effects on strength, arm ergometry performance and psychological well-being. Spinal Cord (2003) 41(1):34–43.10.1038/sj.sc.3101389
    1. Hartkopp A, Harridge SD, Mizuno M, Ratkevicius A, Quistorff B, Kjaer M, et al. Effect of training on contractile and metabolic properties of wrist extensors in spinal cord-injured individuals. Muscle Nerve (2003) 27(1):72–80.10.1002/mus.10290
    1. Glinsky J, Harvey L, Korten M, Drury C, Chee S, Gandevia SC. Short-term progressive resistance exercise may not be effective at increasing wrist strength in people with tetraplegia: a randomised controlled trial. Aust J Physiother (2008) 54(2):103–8.10.1016/S0004-9514(08)70043-6
    1. Urbin MA, Harris-Love ML, Carter AR, Lang CE. High-intensity, unilateral resistance training of a non-paretic muscle group increases active range of motion in a severely paretic upper extremity muscle group after stroke. Front Neurol (2015) 6:119.10.3389/fneur.2015.00119
    1. Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A, et al. International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med (2011) 34(6):535–46.10.1179/107902611X13186000420242
    1. Jebsen R, Taylor N, Trieschmann R, Trotter M, Howard L. An objective and standardised test of hand function. Arch Phys Med Rehabil (1969) 50(6):311–9.
    1. Mayhew JL, Ball TE, Arnold MD, Bowen JC. Relative muscular endurance performance as a predictor of bench press strength in college men and women. J Appl Sport Sci Res (1992) 6(4):200–6.10.1519/00124278-199211000-00002
    1. Bullock IM, Zheng JZ, De La Rosa S, Guertler C, Dollar AM. Grasp frequency and usage in daily household and machine shop tasks. IEEE Trans Haptics (2013) 6(3):296–308.10.1109/TOH.2013.6
    1. Mateo S, Roby-Brami A, Reilly KT, Rossetti Y, Collet C, Rode G. Upper limb kinematics after cervical spinal cord injury: a review. J Neuroeng Rehabil (2015) 12:9.10.1186/1743-0003-12-9
    1. Weinstein S. Fifty years of somatosensory research: from the Semmes-Weinstein monofilaments to the Weinstein Enhanced Sensory Test. J Hand Ther (1993) 6(1):11–22;discussion50.10.1016/S0894-1130(12)80176-1
    1. Halar EM, Hammond MC, LaCava EC, Camann C, Ward J. Sensory perception threshold measurement: an evaluation of semiobjective testing devices. Arch Phys Med Rehabil (1987) 68(8):499–507.
    1. Hasegawa Y, Kasai T, Tsuji T, Yahagi S. Further insight into the task-dependent excitability of motor evoked potentials in first dorsal interosseous muscle in humans. Exp Brain Res (2001) 140(4):387–96.10.1007/s002210100842
    1. Carson RG, Nelson BD, Buick AR, Carroll TJ, Kennedy NC, Cann RM. Characterizing changes in the excitability of corticospinal projections to proximal muscles of the upper limb. Brain Stimul (2013) 6:760–8.10.1016/j.brs.2013.01.016
    1. Liang MH, Fossel AH, Larson MG. Comparisons of five health status instruments for orthopedic evaluation. Med Care (1990) 28(7):632–42.10.1097/00005650-199007000-00008
    1. Cohen J. Statistical Power Analysis for the Behavioural Sciences. New York: Academic Press; (1977).
    1. Dobkin BH. Progressive staging of pilot studies to improve phase III trials for motor interventions. Neurorehabil Neural Repair (2009) 23(3):197–206.10.1177/1545968309331863
    1. Ehrsson HH, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H. Cortical activity in precision-versus power-grip tasks: an fMRI study. J Neurophysiol (2000) 83(1):528–36.
    1. Huesler E, Hepp-Reymond M, Dietz V. Task dependence of muscle synchronization in human hand muscles. Neuroreport (1998) 13(10):2167–70.10.1097/00001756-199807130-00003
    1. Caria MA, Kaneko T, Kimura A, Asanuma H. Functional organization of the projection from area 2 to area 4 g in the cat. J Neurophysiol (1997) 77(6):3107–14.
    1. Cuypers K, Levin O, Thijs H, Swinnen SP, Meesen RL. Long-term TENS treatment improves tactile sensitivity in MS patients. Neurorehabil Neural Repair (2010) 24:420–7.10.1177/1545968309356301
    1. Field-Fote EC, Yang JF, Basso DM, Gorassini MA. Supraspinal control predicts locomotor function and forecasts responsiveness to training after spinal cord injury. J Neurotrauma (2016). Available from:
    1. Long C, Conrad P, Hall E, Furler S. Intrinsic-extrinsic muscle control of the hand in power grip and precision handling. J Bone Joint Surg Am (1970) 52(5):853–67.10.2106/00004623-197052050-00001
    1. Lemon RN, Griffiths J. Comparing the function of the corticospinal system in different species: organizational differences for motor specialization? Muscle Nerve (2005) 32(3):261–79.10.1002/mus.20333
    1. Macé MJ, Levin O, Alaerts K, Rothwell JC, Swinnen SP. Corticospinal facilitation following prolonged proprioceptive stimulation by means of passive wrist movement. J Clin Neurophysiol (2008) 25(4):202–9.10.1097/WNP.0b013e31817da170
    1. Manella KJ, Torres J, Field-Fote EC. Restoration of walking function in an individual with chronic complete (AIS A) spinal cord injury. J Rehabil Med (2010) 42(8):795–8.10.2340/16501977-0593

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