Advertisement

Synergistic Control of Hand Muscles Through Common Neural Input

  • Marco Santello
Chapter
Part of the Springer Tracts in Advanced Robotics book series (STAR, volume 95)

Abstract

Skilled grasping and manipulation rely on spatial and temporal coordination of multiple hand muscles. This chapter describes the phenomenon of common neural input to hand muscles as one of the mechanisms through which the Central Nervous system might coordinate the neural activation of groups of hand muscles acting on a single or multiple digits. The heterogeneous distribution of common input to intrinsic and extrinsic hand muscles is discussed in relation to its functional role for the coordination of hand muscles.

Keywords

Synchrony Coherence Motor units EMG 

Notes

Acknowledgments

Marco Santello thanks Drs. Thomas Hamm, Brach Poston, and Mark Jesunathadas for their valuable comments on the chapter.

References

  1. 1.
    E. Pierrot-Deseilligny, D. Burke, The Circuitry of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders, vol 129 (Cambridge University Press, Cambridge, 2005), pp. 551–554 (ISBN: 978-0-521-82581-8 Brain Feb. 2006)Google Scholar
  2. 2.
    M.R. Caccia, A.J. McComas, A.R. Upton, T. Blogg, Cutaneous reflexes in small muscles of the hand. J. Neurol. Neurosurg. Psychiatry 36, 960–977 (1973)CrossRefGoogle Scholar
  3. 3.
    R. Chen, P. Ashby, Reflex responses in upper limb muscles to cutaneous stimuli. Can. J. Neurol. Sci. 20, 271–278 (1993)MATHGoogle Scholar
  4. 4.
    R. Garnett, J.A. Stephens, The reflex responses of single motor units in human first dorsal interosseous muscle following cutaneous afferent stimulation. J. Physiol. 303, 351–364 (1980)Google Scholar
  5. 5.
    C.J. De Luca, B. Mambrito, Voluntary control of motor units in human antagonist muscles: coactivation and reciprocal activation. J. Neurophysiol. 58, 525–542 (1987)Google Scholar
  6. 6.
    C.J. De Luca, A.M. Roy, Z. Erim, Synchronization of motor-unit firings in several human muscles. J. Neurophysiol. 70, 2010–2023 (1993)Google Scholar
  7. 7.
    C.J. De Luca, Z. Erim, Common drive of motor units in regulation of muscle force. Trends Neurosci. 17, 299–305 (1994)CrossRefGoogle Scholar
  8. 8.
    A. Adam, C.J. De Luca, Z. Erim, Hand dominance and motor unit firing behavior. J. Neurophysiol. 80, 1373–1382 (1998)Google Scholar
  9. 9.
    C.J. De Luca, Z. Erim, Common drive in motor units of a synergistic muscle pair. J. Neurophysiol. 87, 2200–2204 (2002)Google Scholar
  10. 10.
    M.M. Lowery, Z. Erim, A simulation study to examine the effect of common motoneuron inputs on correlated patterns of motor unit discharge. J. Comput. Neurosci. 19, 107–124 (2005)CrossRefMATHGoogle Scholar
  11. 11.
    D.H. Perkel, G.L. Gerstein, G.P. Moore, Neuronal spike trains and stochastic point processes I. The single spike train. Biophys. J. 7, 391–418 (1967)CrossRefGoogle Scholar
  12. 12.
    D.H. Perkel, G.L. Gerstein, G.P. Moore, Neuronal spike trains and stochastic point processes II. Simultaneous spike trains. Biophys. J. 7, 419–440 (1967)CrossRefGoogle Scholar
  13. 13.
    M.A. Nordstrom, A.J. Fuglevand, R.M. Enoka, Estimating the strength of common input to human motoneurons from the cross-correlogram. J. Physiol. 453, 547–574 (1992)Google Scholar
  14. 14.
    P.A. Kirkwood, T.A. Sears, The synaptic connexions to intercostal motoneurones as revealed by the average common excitation potential. J. Physiol. 275, 103–134 (1978)Google Scholar
  15. 15.
    T.A. Sears, D. Stagg, Short-term synchronization of intercostal motoneurone activity. J. Physiol. 263, 357–381 (1976)Google Scholar
  16. 16.
    P.A. Kirkwood, On the use and interpretation of cross-correlations measurements in the mammalian central nervous system. J. Neurosci. Methods 1, 107–132 (1979)CrossRefGoogle Scholar
  17. 17.
    P.H. Ellaway, K.S. Murthy, The source and distribution of short-term synchrony between gamma-motoneurones in the cat. Q. J. Exp. Physiol. 70, 233–247 (1985)Google Scholar
  18. 18.
    M.D. Binder, R.K. Powers, Relationship between simulated common synaptic input and discharge synchrony in cat spinal motoneurons. J. Neurophysiol. 86, 2266–2275 (2001)Google Scholar
  19. 19.
    A.M. Taylor, R.M. Enoka, Quantification of the factors that influence discharge correlation in model motor neurons. J. Neurophysiol. 91, 796–814 (2004)CrossRefGoogle Scholar
  20. 20.
    A.M. Taylor, R.M. Enoka, Optimization of input patterns and neuronal properties to evoke motor neuron synchronization. J. Comput. Neurosci. 16, 139–157 (2004)CrossRefGoogle Scholar
  21. 21.
    G.P. Moore, D.H. Perkel, J.P. Segundo, Statistical analysis and functional interpretation of neuronal spike data. Annu. Rev. Physiol. 28, 493–522 (1966)CrossRefGoogle Scholar
  22. 22.
    S.F. Farmer, F.D. Bremner, D.M. Halliday, J.R. Rosenberg, J.A. Stephens, The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J. Physiol. 470, 127–155 (1993)Google Scholar
  23. 23.
    J.R. Rosenberg, D.M. Halliday, P. Breeze, B.A. Conway, Identification of patterns of neuronal connectivity–partial spectra, partial coherence, and neuronal interactions. J. Neurosci. Methods 83, 57–72 (1998)CrossRefGoogle Scholar
  24. 24.
    D.M. Halliday, Weak, stochastic temporal correlation of large scale synaptic input is A major determinant of neuronal bandwidth. Neural Comput. 12, 693–707 (2000)CrossRefGoogle Scholar
  25. 25.
    J.R. Rosenberg, A.M. Amjad, P. Breeze, D.R. Brillinger, D.M. Halliday, The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog. Biophys. Mol. Biol. 53, 1–31 (1989)CrossRefGoogle Scholar
  26. 26.
    J.A. Johnston, G. Formicone, T.M. Hamm, M. Santello, Assessment of across-muscle coherence using multi-unit versus single-unit recordings. Exp. Brain Res. 207, 269–282 (2010)CrossRefGoogle Scholar
  27. 27.
    J.A. Johnston, S.A. Winges, M. Santello, Periodic modulation of motor-unit activity in extrinsic hand muscles during multidigit grasping. J. Neurophysiol. 94, 206–218 (2005)CrossRefGoogle Scholar
  28. 28.
    J.G. Semmler, K.W. Kornatz, D.V. Dinenno, S. Zhou, R.M. Enoka, Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J. Physiol. 545, 681–695 (2002)CrossRefGoogle Scholar
  29. 29.
    J.G. Semmler, K.W. Kornatz, R.M. Enoka, Motor-unit coherence during isometric contractions is greater in a hand muscle of older adults. J. Neurophysiol. 90, 1346–1349 (2003)CrossRefGoogle Scholar
  30. 30.
    S.A. Winges, J.A. Johnston, M. Santello, Muscle-pair specific distribution and grip-type modulation of neural common input to extrinsic digit flexors. J. Neurophysiol. 96, 1258–1266 (2006)CrossRefGoogle Scholar
  31. 31.
    J.G. Semmler, M.A. Nordstrom, C.J. Wallace, Relationship between motor unit short-term synchronization and common drive in human first dorsal interosseous muscle. Brain Res. 767, 314–320 (1997)CrossRefGoogle Scholar
  32. 32.
    J.G. Semmler, M.V. Sale, F.G. Meyer, M.A. Nordstrom, Motor-unit coherence and its relation with synchrony are influenced by training. J. Neurophysiol. 92, 3320–3331 (2004)CrossRefGoogle Scholar
  33. 33.
    C.T. Moritz, E.A. Christou, F.G. Meyer, R.M. Enoka, Coherence at 16–32 Hz can be caused by short-term synchrony of motor units. J. Neurophysiol. 94, 105–118 (2005)CrossRefGoogle Scholar
  34. 34.
    M.M. Lowery, L.J. Myers, Z. Erim, Coherence between motor unit discharges in response to shared neural inputs. J. Neurosci. Methods 163, 384–391 (2007)CrossRefGoogle Scholar
  35. 35.
    A.K. Datta, J.A. Stephens, Synchronization of motor unit activity during voluntary contraction in man. J. Physiol. 422, 397–419 (1990)Google Scholar
  36. 36.
    F.D. Bremner, J.R. Baker, J.A. Stephens, Variation in the degree of synchronization exhibited by motor units lying in different finger muscles in man. J. Physiol. 432, 381–399 (1991)Google Scholar
  37. 37.
    F.D. Bremner, J.R. Baker, J.A. Stephens, Correlation between the discharges of motor units recorded from the same and from different finger muscles in man. J. Physiol. 432, 355–380 (1991)Google Scholar
  38. 38.
    J. Gibbs, L.M. Harrison, J.A. Stephens, Organization of inputs to motoneurone pools in man. J. Physiol. 485(Pt 1), 245–256 (1995)Google Scholar
  39. 39.
    E.J. Huesler, M.A. Maier, M.C. Hepp-Reymond, EMG activation patterns during force production in precision grip. III. Synchronisation of single motor units. Exp. Brain Res. 134, 441–455 (2000)CrossRefGoogle Scholar
  40. 40.
    D.A. Keen, A.J. Fuglevand, Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. J. Neurophysiol. 91, 57–62 (2004)CrossRefGoogle Scholar
  41. 41.
    K.T. Reilly, M.H. Schieber, Incomplete functional subdivision of the human multitendoned finger muscle flexor digitorum profundus: an electromyographic study. J. Neurophysiol. 90, 2560–2570 (2003)CrossRefGoogle Scholar
  42. 42.
    K.T. Reilly, M.A. Nordstrom, M.H. Schieber, Short-term synchronization between motor units in different functional subdivisions of the human flexor digitorum profundus muscle. J. Neurophysiol. 92, 734–742 (2004)CrossRefGoogle Scholar
  43. 43.
    S.L. Kilbreath, S.C. Gandevia, Limited independent flexion of the thumb and fingers in human subjects. J. Physiol. 479(Pt 3), 487–497 (1994)Google Scholar
  44. 44.
    V.M. Zatsiorsky, Z.M. Li, M.L. Latash, Enslaving effects in multi-finger force production. Exp. Brain Res. 131, 187–195 (2000)CrossRefGoogle Scholar
  45. 45.
    T.J. Butler, S.L. Kilbreath, R.B. Gorman, S.C. Gandevia, Selective recruitment of single motor units in human flexor digitorum superficialis muscle during flexion of individual fingers. J. Physiol. 567, 301–309 (2005)CrossRefGoogle Scholar
  46. 46.
    H. van Duinen, W.S. Yu, S.C. Gandevia, Limited ability to extend the digits of the human hand independently with extensor digitorum. J. Physiol. 587, 4799–4810 (2009)CrossRefGoogle Scholar
  47. 47.
    W.S. Yu, H. van Duinen, S.C. Gandevia, Limits to the control of the human thumb and fingers in flexion and extension. J. Neurophysiol. 103, 278–289 (2010)CrossRefGoogle Scholar
  48. 48.
    S.A. Winges, K.W. Kornatz, M. Santello, Common input to motor units of intrinsic and extrinsic hand muscles during two-digit object hold. J. Neurophysiol. 99, 1119–1126 (2008)CrossRefGoogle Scholar
  49. 49.
    M. Santello, J.F. Soechting, Force synergies for multifingered grasping. Exp. Brain Res. 133, 457–467 (2000)CrossRefGoogle Scholar
  50. 50.
    M.P. Rearick, A. Casares, M. Santello, Task-dependent modulation of multi-digit force coordination patterns. J. Neurophysiol. 89, 1317–1326 (2003)CrossRefGoogle Scholar
  51. 51.
    G.B. Hockensmith, S.Y. Lowell, A.J. Fuglevand, Common input across motor nuclei mediating precision grip in humans. J. Neurosci. Off. J. Soc. Neurosci. 25, 4560–4564 (2005)Google Scholar
  52. 52.
    S.A. Winges, M. Santello, Common input to motor units of digit flexors during multi-digit grasping. J. Neurophysiol. 92, 3210–3220 (2004)CrossRefGoogle Scholar
  53. 53.
    T.L. McIsaac, A.J. Fuglevand, Common synaptic input across motor nuclei supplying intrinsic muscles involved in the precision grip. Exp. Brain Res. 188, 159–164 (2008)CrossRefGoogle Scholar
  54. 54.
    W.S. Yu, S.L. Kilbreath, R.C. Fitzpatrick, S.C. Gandevia, Thumb and finger forces produced by motor units in the long flexor of the human thumb. J. Physiol. 583, 1145–1154 (2007)CrossRefGoogle Scholar
  55. 55.
    A. Danna-Dos Santos, B. Poston, M. Jesunathadas, L.R. Bobich, T.M. Hamm, M. Santello, Influence of fatigue on hand muscle coordination and EMG–EMG coherence during three-digit grasping. J. Neurophysiol. 104, 3576–3587 (2010)CrossRefGoogle Scholar
  56. 56.
    B. Poston, A. Danna-Dos Santos, M. Jesunathadas, T.M. Hamm, M. Santello, Force-independent distribution of correlated neural inputs to hand muscles during three-digit grasping. J. Neurophysiol. 104, 1141–1154 (2010)CrossRefGoogle Scholar
  57. 57.
    F.D. Bremner, J.R. Baker, J.A. Stephens, Effect of task on the degree of synchronization of intrinsic hand muscle motor units in man. J. Neurophysiol. 66, 2072–2083 (1991)Google Scholar
  58. 58.
    E.J. Huesler, M.C. Hepp-Reymond, V. Dietz, Task dependence of muscle synchronization in human hand muscles. NeuroReport 9, 2167–2170 (1998)CrossRefGoogle Scholar
  59. 59.
    D.J. Kidgell, M.V. Sale, J.G. Semmler, Motor unit synchronization measured by cross-correlation is not influenced by short-term strength training of a hand muscle. Exp. Brain Res. 175, 745–753 (2006)CrossRefGoogle Scholar
  60. 60.
    C.M. Gray, Synchronous oscillations in neuronal systems: mechanisms and functions. J. Comput. Neurosci. 1, 11–38 (1994)CrossRefGoogle Scholar
  61. 61.
    S.F. Farmer, Rhythmicity, synchronization and binding in human and primate motor systems. J. Physiol. 509(Pt 1), 3–14 (1998)Google Scholar
  62. 62.
    J.H. McAuley, C.D. Marsden, Physiological and pathological tremors and rhythmic central motor control. Brain J. Neurol. 123(Pt 8), 1545–1567 (2000)CrossRefGoogle Scholar
  63. 63.
    J.M. Kilner, M. Alonso–Alonso, R. Fisher, R.N. Lemon, Modulation of synchrony between single motor units during precision grip tasks in humans. J. Physiol. 541, 937–948 (2002)CrossRefGoogle Scholar
  64. 64.
    J.M. Kilner, S. Salenius, S.N. Baker, A. Jackson, R. Hari, R.N. Lemon, Task-dependent modulations of cortical oscillatory activity in human subjects during a bimanual precision grip task. NeuroImage 18, 67–73 (2003)CrossRefGoogle Scholar
  65. 65.
    N. Kakuda, M. Nagaoka, J. Wessberg, Common modulation of motor unit pairs during slow wrist movement in man. J. Physiol. 520(Pt 3), 929–940 (1999)CrossRefGoogle Scholar
  66. 66.
    T.L. McIsaac, A.J. Fuglevand, Influence of tactile afferents on the coordination of muscles during a simulated precision grip. Exp. Brain Res. 174, 769–774 (2006)CrossRefGoogle Scholar
  67. 67.
    R.J. Fisher, M.P. Galea, P. Brown, R.N. Lemon, Digital nerve anaesthesia decreases EMG–EMG coherence in a human precision grip task. Exp. Brain Res. 145, 207–214 (2002)CrossRefGoogle Scholar
  68. 68.
    T.L. McIsaac, A.J. Fuglevand, Motor-unit synchrony within and across compartments of the human flexor digitorum superficialis. J. Neurophysiol. 97, 550–556 (2007)CrossRefGoogle Scholar
  69. 69.
    J.L. Taylor, S.C. Gandevia, A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J. Appl. Physiol. (Bethesda, Md.: 1985) 104, 542–550 (2008)Google Scholar
  70. 70.
    M. Santello, A.J. Fuglevand, Role of across-muscle motor unit synchrony for the coordination of forces. Exp. Brain Res. 159, 501–508 (2004)CrossRefGoogle Scholar
  71. 71.
    M.P. Rearick, M. Santello, Force synergies for multifingered grasping: effect of predictability in object center of mass and handedness. Exp. Brain Res. 144, 38–49 (2002)Google Scholar
  72. 72.
    M.P. Rearick, G.E. Stelmach, B. Leis, M. Santello, Coordination and control of forces during multifingered grasping in Parkinson’s disease. Exp. Neurol. 177, 428–442 (2002)CrossRefGoogle Scholar
  73. 73.
    A.J. Fuglevand, D.A. Winter, A.E. Patla, D. Stashuk, Detection of motor unit action potentials with surface electrodes: influence of electrode size and spacing. Biol. Cybern. 67, 143–153 (1992)CrossRefGoogle Scholar
  74. 74.
    A.J. Fuglevand, D.A. Winter, A.E. Patla, Models of recruitment and rate coding organization in motor-unit pools. J. Neurophysiol. 70, 2470–2488 (1993)Google Scholar
  75. 75.
    M.C. Tresch, A. Jarc, The case for and against muscle synergies. Curr. Opin. Neurobiol. 19, 601–607 (2009)CrossRefGoogle Scholar
  76. 76.
    S.A. Overduin, A. d’Avella, J. Roh, E. Bizzi, Modulation of muscle synergy recruitment in primate grasping. J. Neurosci. Off. J. Soc. Neurosci. 28, 880–892 (2008)CrossRefGoogle Scholar
  77. 77.
    J.G. Semmler, Motor unit synchronization and neuromuscular performance. Exerc. Sport Sci. Rev. 30, 8–14 (2002)CrossRefGoogle Scholar
  78. 78.
    F.J. Valero-Cuevas, Predictive modulation of muscle coordination pattern magnitude scales fingertip force magnitude over the voluntary range. J. Neurophysiol. 83, 1469–1479 (2000)Google Scholar
  79. 79.
    F.J. Valero-Cuevas, F.E. Zajac, C.G. Burgar, Large index-fingertip forces are produced by subject-independent patterns of muscle excitation. J. Biomech. 31, 693–703 (1998)CrossRefGoogle Scholar
  80. 80.
    J.A. Johnston, L.R. Bobich, M. Santello, Coordination of intrinsic and extrinsic hand muscle activity as a function of wrist joint angle during two-digit grasping. Neurosci. Lett. 474, 104–108 (2010)CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.School of Biological and Health Systems EngineeringArizona State UniversityTempeUSA

Personalised recommendations