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Modulation of hand aperture during reaching in persons with incomplete cervical spinal cord injury

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Abstract

The intact neuromotor system prepares for object grasp by first opening the hand to an aperture that is scaled according to object size and then closing the hand around the object. After cervical spinal cord injury (SCI), hand function is significantly impaired, but the degree to which object-specific hand aperture scaling is affected remains unknown. Here, we hypothesized that persons with incomplete cervical SCI have a reduced maximum hand opening capacity but exhibit novel neuromuscular coordination strategies that permit object-specific hand aperture scaling during reaching. To test this hypothesis, we measured hand kinematics and surface electromyography from seven muscles of the hand and wrist during attempts at maximum hand opening as well as reaching for four balls of different diameters. Our results showed that persons with SCI exhibited significantly reduced maximum hand aperture compared to able-bodied (AB) controls. However, persons with SCI preserved the ability to scale peak hand aperture with ball size during reaching. Persons with SCI also used distinct muscle coordination patterns that included increased co-activity of flexors and extensors at the wrist and hand compared to AB controls. These results suggest that motor planning for aperture modulation is preserved even though execution is limited by constraints on hand opening capacity and altered muscle co-activity. Thus, persons with incomplete cervical SCI may benefit from rehabilitation aimed at increasing hand opening capacity and reducing flexor–extensor co-activity at the wrist and hand.

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References

  • Alberts JL, Saling M, Adler CH, Stelmach GE (2000) Disruptions in the reach-to-grasp actions of Parkinson’s patients. Exp Brain Res 134:353–362

    Article  CAS  PubMed  Google Scholar 

  • Alstermark B, Isa T, Pettersson LG, Sasaki S (2007) The C3-C4 propriospinal system in the cat and monkey: a spinal pre-motoneuronal centre for voluntary motor control. Acta Physiol (Oxf) 189:123–140. doi:10.1111/j.1748-1716.2006.01655.x

    Article  CAS  Google Scholar 

  • Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7:269–277. doi:10.1038/nn1195

    Article  CAS  PubMed  Google Scholar 

  • Beekhuizen KS, Field-Fote EC (2005) 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 19:33–45. doi:10.1177/1545968305274517

    Article  PubMed  Google Scholar 

  • Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund HJ (1998) Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology 50:1253–1259

    Article  CAS  PubMed  Google Scholar 

  • Bruehlmeier M, Dietz V, Leenders KL, Roelcke U, Missimer J, Curt A (1998) How does the human brain deal with a spinal cord injury? Eur J Neurosci 10:3918–3922

    Article  CAS  PubMed  Google Scholar 

  • Castiello U (2005) The neuroscience of grasping. Nat Rev Neurosci 6:726–736. doi:10.1038/nrn1744

    Article  CAS  PubMed  Google Scholar 

  • Cavanagh PR, Komi PV (1979) Electromechanical delay in human skeletal muscle under concentric and eccentric contractions. Eur J Appl Physiol Occup Physiol 42:159–163

    Article  CAS  PubMed  Google Scholar 

  • Darian-Smith I, Burman K, Darian-Smith C (1999) Parallel pathways mediating manual dexterity in the macaque. Exp Brain Res 128:101–108

    Article  CAS  PubMed  Google Scholar 

  • Delagi EF, Perotto A (1979) Anatomical guide for the electromyographer. Charles C Thomas, Springfield

    Google Scholar 

  • Di Rienzo F, Guillot A, Mateo S, Daligault S, Delpuech C, Rode G, Collet C (2014) Neuroplasticity of prehensile neural networks after quadriplegia. Neuroscience 274:82–92. doi:10.1016/j.neuroscience.2014.05.021

    Article  PubMed  Google Scholar 

  • Edgerton VR, Kim SJ, Ichiyama RM, Gerasimenko YP, Roy RR (2006) Rehabilitative therapies after spinal cord injury. J Neurotrauma 23:560–570. doi:10.1089/neu.2006.23.560

    Article  PubMed  Google Scholar 

  • Enoka RM (1997) Neural strategies in the control of muscle force. Muscle Nerve Suppl 5:S66–S69

    Article  CAS  PubMed  Google Scholar 

  • Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G (2001) Cortical mechanism for the visual guidance of hand grasping movements in the monkey: a reversible inactivation study. Brain 124:571–586

    Article  CAS  PubMed  Google Scholar 

  • Fouad K, Dietz V, Schwab ME (2001) Improving axonal growth and functional recovery after experimental spinal cord injury by neutralizing myelin associated inhibitors. Brain Res Brain Res Rev 36:204–212

    Article  CAS  PubMed  Google Scholar 

  • Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. NeuroReport 5:1525–1529

    Article  CAS  PubMed  Google Scholar 

  • Girgis J, Merrett D, Kirkland S, Metz GA, Verge V, Fouad K (2007) Reaching training in rats with spinal cord injury promotes plasticity and task specific recovery. Brain 130:2993–3003. doi:10.1093/brain/awm245

    Article  CAS  PubMed  Google Scholar 

  • Green JB, Sora E, Bialy Y, Ricamato A, Thatcher RW (1999) Cortical motor reorganization after paraplegia: an EEG study. Neurology 53:736–743

    Article  CAS  PubMed  Google Scholar 

  • Haggard P, Wing A (1998) Coordination of hand aperture with the spatial path of hand transport. Exp Brain Res 118:286–292

    Article  CAS  PubMed  Google Scholar 

  • Harvey LA, Batty J, Jones R, Crosbie J (2001) Hand function of C6 and C7 tetraplegics 1–16 years following injury. Spinal Cord 39:37–43. doi:10.1038/sj.sc.3101101

    Article  CAS  PubMed  Google Scholar 

  • Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374

    Article  CAS  PubMed  Google Scholar 

  • Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In: Baddeley RLA (ed) Attention and performance IX. Erlbaum Associates, Hillsdale, pp 153–169

    Google Scholar 

  • Jeannerod M (1986) The formation of finger grip during prehension: a cortically mediated visuomotor pattern. Behav Brain Res 19:99–116. doi:10.1016/0166-4328(86)90008-2

    Article  CAS  PubMed  Google Scholar 

  • Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA (1969) An objective and standardized test of hand function. Arch Phys Med Rehabil 50:311–319

    CAS  PubMed  Google Scholar 

  • Kapadia N, Zivanovic V, Popovic MR (2013) Restoring voluntary grasping function in individuals with incomplete chronic spinal cord injury: pilot study. Top Spinal Cord Inj Rehabil 19:279–287. doi:10.1310/sci1904-279

    Article  PubMed Central  PubMed  Google Scholar 

  • Koshland GF, Galloway JC, Farley B (2005) Novel muscle patterns for reaching after cervical spinal cord injury: a case for motor redundancy. Exp Brain Res 164:133–147. doi:10.1007/s00221-005-2218-9

    Article  PubMed  Google Scholar 

  • Laffont I, Briand E, Dizien O, Combeaud M, Bussel B, Revol M, Roby-Brami A (2000) Kinematics of prehension and pointing movements in C6 quadriplegic patients. Spinal Cord 38:354–362

    Article  CAS  PubMed  Google Scholar 

  • Laffont I, Hoffmann G, Dizien O, Revol M, Roby-Brami A (2007) How do C6/C7 tetraplegic patients grasp balls of different sizes and weights? Impact of surgical musculo-tendinous transfers. Spinal Cord 45:502–512. doi:10.1038/sj.sc.3102047

    Article  CAS  PubMed  Google Scholar 

  • Lang CE, Schieber MH (2004) Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. J Neurophysiol 91:1722–1733. doi:10.1152/jn.00805.2003

    Article  PubMed  Google Scholar 

  • Latash ML, Friedman J, Kim SW, Feldman AG, Zatsiorsky VM (2010) Prehension synergies and control with referent hand configurations. Exp Brain Res 202:213–229. doi:10.1007/s00221-009-2128-3

    Article  PubMed Central  PubMed  Google Scholar 

  • Levene H (1960) Robust tests for equality of variances, in contributions to probability and statistics. Stanford University Press, Palo Alto

    Google Scholar 

  • Marciniak C, Rader L, Gagnon C (2008) The use of botulinum toxin for spasticity after spinal cord injury. Am J Phys Med Rehabil 87:312–317. doi:10.1097/PHM.0b013e318168ceaf quiz 318-320, 329

    Article  PubMed  Google Scholar 

  • Marino RJ, Ditunno JF Jr, Donovan WH, Maynard F Jr (1999) Neurologic recovery after traumatic spinal cord injury: data from the Model Spinal Cord Injury Systems. Arch Phys Med Rehabil 80:1391–1396

    Article  CAS  PubMed  Google Scholar 

  • Marteniuk RG, Leavitt JL, Mackenzie CL, Athenes S (1990) Functional-relationships between grasp and transport components in a prehension task. Hum Mov Sci 9:149–176. doi:10.1016/0167-9457(90)90025-9

    Article  Google Scholar 

  • Mateo S, Revol P, Fourtassi M, Rossetti Y, Collet C, Rode G (2013) Kinematic characteristics of tenodesis grasp in C6 quadriplegia. Spinal Cord 51:144–149. doi:10.1038/sc.2012.101

    Article  CAS  PubMed  Google Scholar 

  • Michaelsen SM, Magdalon EC, Levin MF (2009) Grip aperture scaling to object size in chronic stroke. Motor Control 13:197–217

    PubMed  Google Scholar 

  • Muir RB, Lemon RN (1983) Corticospinal neurons with a special role in precision grip. Brain Res 261:312–316

    Article  CAS  PubMed  Google Scholar 

  • Osu R, Franklin DW, Kato H, Gomi H, Domen K, Yoshioka T, Kawato M (2002) Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. J Neurophysiol 88:991–1004

    PubMed  Google Scholar 

  • Oudega M, Perez MA (2012) Corticospinal reorganization after spinal cord injury. J Physiol 590:3647–3663. doi:10.1113/jphysiol.2012.233189

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pettersson LG, Alstermark B, Blagovechtchenski E, Isa T, Sasaski S (2007) Skilled digit movements in feline and primate–recovery after selective spinal cord lesions. Acta Physiol (Oxf) 189:141–154. doi:10.1111/j.1748-1716.2006.01650.x

    Article  CAS  Google Scholar 

  • Pierrot-Deseilligny E (1996) Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneurons. Prog Neurobiol 48:489–517

    Article  CAS  PubMed  Google Scholar 

  • Platz T, Pinkowski C, van Wijck F, Kim IH, di Bella P, Johnson G (2005) Reliability and validity of arm function assessment with standardized guidelines for the Fugl-Meyer test, action research arm test and box and block test: a multicentre study. Clin Rehabil 19:404–411

    Article  PubMed  Google Scholar 

  • Popovic MR, Thrasher TA, Adams ME, Takes V, Zivanovic V, Tonack MI (2006) Functional electrical therapy: retraining grasping in spinal cord injury. Spinal Cord 44:143–151. doi:10.1038/sj.sc.3101822

    Article  CAS  PubMed  Google Scholar 

  • Ragnarsson KT (2008) Functional electrical stimulation after spinal cord injury: current use, therapeutic effects and future directions. Spinal Cord 46:255–274. doi:10.1038/sj.sc.3102091

    Article  CAS  PubMed  Google Scholar 

  • Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2:263–273. doi:10.1038/35067570

    Article  CAS  PubMed  Google Scholar 

  • Rand MK, Smiley-Oyen AL, Shimansky YP, Bloedel JR, Stelmach GE (2006) Control of aperture closure during reach-to-grasp movements in Parkinson’s disease. Exp Brain Res 168:131–142. doi:10.1007/s00221-005-0073-3

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Selen LP, Beek PJ, van Dieen JH (2006) Impedance is modulated to meet accuracy demands during goal-directed arm movements. Exp Brain Res 172:129–138. doi:10.1007/s00221-005-0320-7

    Article  PubMed  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611. doi:10.2307/2333709

    Article  Google Scholar 

  • Topka H, Cohen LG, Cole RA, Hallett M (1991) Reorganization of corticospinal pathways following spinal cord injury. Neurology 41:1276–1283

    Article  CAS  PubMed  Google Scholar 

  • Trumbower RD, Ravichandran VJ, Krutky MA, Perreault EJ (2010) Contributions of altered stretch reflex coordination to arm impairments following stroke. J Neurophysiol 104:3612–3624. doi:10.1152/jn.00804.2009

    Article  PubMed Central  PubMed  Google Scholar 

  • Weiss EJ, Flanders M (2004) Muscular and postural synergies of the human hand. J Neurophysiol 92:523–535. doi:10.1152/jn.01265.2003

    Article  PubMed  Google Scholar 

  • Wrigley PJ, Gustin SM, Macey PM et al (2009) Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cereb Cortex 19:224–232. doi:10.1093/cercor/bhn072

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by NIH Grant K12 HD055931 and Craig H. Neilsen Foundation. The authors are very grateful to the participants. The authors would also like to thank Ian Cooke, Matthew Freeman, and Dennis Valerstain for their assistance with data collection.

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Correspondence to Randy D. Trumbower.

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Victoria Stahl and Heather B Hayes have contributed equally to this work.

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Stahl, V.A., Hayes, H.B., Buetefisch, C.M. et al. Modulation of hand aperture during reaching in persons with incomplete cervical spinal cord injury. Exp Brain Res 233, 871–884 (2015). https://doi.org/10.1007/s00221-014-4163-y

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