Experimental Brain Research

, Volume 190, Issue 3, pp 347–359 | Cite as

A spinal pathway between synergists can modulate activity in human elbow flexor muscles

  • Benjamin K. BarryEmail author
  • Zachary A. Riley
  • Michael A. Pascoe
  • Roger M. Enoka
Research Article


Electrical stimulation of the brachioradialis branch of the radial nerve has been shown to inhibit the discharge of voluntarily activated motor units in biceps brachii during weak contractions with the elbow flexor muscles. The purpose of the present study was to characterise the inhibitory reflex by comparing its strength in the short and long heads of the biceps brachii and examining the influence of forearm position on the strength of the reflex. Spike-triggered stimulation was used to assess the influence of radial nerve stimulation on the discharge of single motor units in the biceps brachii of 15 subjects. Stimulation of the radial nerve prolonged the interspike interval (P < 0.001) of motor units in the long (n = 31, 4.8 ± 5.6 ms) and short heads (n = 26, 8.1 ± 12.3 ms) of biceps brachii with no difference between the two heads (P = 0.11). The strength of inhibition varied with forearm position for motor units in both heads (n = 18, P < 0.05). The amount of inhibition was greatest in pronation (7.9 ± 8.9 ms), intermediate in neutral (5.8 ± 7.1 ms), and least in supination (2.8 ± 3.4 ms). These findings indicate that the inhibition evoked by afferent feedback from brachioradialis to low-threshold motor units (mean force 3–5% MVC) in biceps brachii varied with forearm posture yet was similar for the two heads of biceps brachii. This reflex pathway provides a mechanism to adjust the activation of biceps brachii with changes in forearm position, and represents a spinal basis for a muscle synergy in humans.


Motor unit Inhibition Biceps brachii Brachioradialis Synergy 



Brian J. Paulson, Elizabeth Terry, and Kristin E. Taylor assisted with data collection and analysis. This research was supported by NIH/NINDS NS43275 to RME.


  1. Athwal GS, Steinmann SP, Rispoli DM (2007) The distal biceps tendon: footprint and relevant clinical anatomy. J Hand Surg [Am] 32:1225–1229CrossRefGoogle Scholar
  2. Baldissera F, Bellani G, Cavallari P, Lalli S (2000) Changes in the excitability of the H-reflex in wrist flexors related to the prone or supine position of the forearm in man. Neurosci Lett 295:105–108PubMedCrossRefGoogle Scholar
  3. Barry BK, Carson RG (2004) Transfer of resistance training to enhance rapid coordinated force production by older adults. Exp Brain Res 159:225–238PubMedCrossRefGoogle Scholar
  4. Barry BK, Pascoe MA, Jesunathadas M, Enoka RM (2007) Rate coding is compressed but variability is unaltered for motor units in a hand muscle of old adults. J Neurophysiol 97:3206–3218PubMedCrossRefGoogle Scholar
  5. Basmajian JV, Latif A (1957) Integrated actions and functions of the chief fexors of the elbow: a detailed electromyographic analysis. J Bone Joint Surg Am 39:1106–1118PubMedGoogle Scholar
  6. Blackburn SC, Wood CP, Evans DJ, Watt DJ (2007) Radial nerve contribution to brachialis in the UK Caucasian population: position is predictable based on surface landmarks. Clin Anat 20:64–67PubMedCrossRefGoogle Scholar
  7. Buchanan TS, Almdale DP, Lewis JL, Rymer WZ (1986) Characteristics of synergic relations during isometric contractions of human elbow muscles. J Neurophysiol 56:1225–1241PubMedGoogle Scholar
  8. Buchanan TS, Rovai GP, Rymer WZ (1989) Strategies for muscle activation during isometric torque generation at the human elbow. J Neurophysiol 62:1201–1212PubMedGoogle Scholar
  9. Burke D, Gracies JM, Meunier S, Pierrot-Deseilligny E (1992) Changes in presynaptic inhibition of afferents to propriospinal-like neurones in man during voluntary contractions. J Physiol 449:673–687PubMedGoogle Scholar
  10. Cavallari P, Katz R (1989) Pattern of projections of group I afferents from forearm muscles to motoneurones supplying biceps and triceps muscles in man. Exp Brain Res 78:465–478PubMedCrossRefGoogle Scholar
  11. Datta AK, Stephens JA (1981) The effects of digital nerve stimulation on the firing of motor units in human first dorsal interosseous muscle. J Physiol 318:501–510PubMedGoogle Scholar
  12. Eames MH, Bain GI, Fogg QA, van Riet RP (2007) Distal biceps tendon anatomy: a cadaveric study. J Bone Joint Surg Am 89:1044–1049PubMedCrossRefGoogle Scholar
  13. Ellaway PH (1978) Cumulative sum technique and its application to the analysis of peristimulus time histograms. Electroencephalogr Clin Neurophysiol 45:302–304PubMedCrossRefGoogle Scholar
  14. Fournier E, Meunier S, Pierrot-Deseilligny E, Shindo M (1986) Evidence for interneuronally mediated Ia excitatory effects to human quadriceps motoneurones. J Physiol 377:143–169PubMedGoogle Scholar
  15. Gielen CC, van Zuylen EJ (1986) Coordination of arm muscles during flexion and supination: application of the tensor analysis approach. Neuroscience 17:527–539PubMedCrossRefGoogle Scholar
  16. Herrmann U, Flanders M (1998) Directional tuning of single motor units. J Neurosci 18:8402–8416PubMedGoogle Scholar
  17. Hultborn H, Meunier S, Morin C, Pierrot-Deseilligny E (1987) Assessing changes in presynaptic inhibition of I a fibres: a study in man and the cat. J Physiol 389:729–756PubMedGoogle Scholar
  18. Jamison JC, Caldwell GE (1993) Muscle synergies and isometric torque production: influence of supination and pronation level on elbow flexion. J Neurophysiol 70:947–960PubMedGoogle Scholar
  19. Jongen HA, Denier van der Gon JJ, Gielen CC (1989) Inhomogeneous activation of motoneurone pools as revealed by co-contraction of antagonistic human arm muscles. Exp Brain Res 75:555–562Google Scholar
  20. Katz R, Penicaud A, Rossi A (1991) Reciprocal Ia inhibition between elbow flexors and extensors in the human. J Physiol 437:269–286PubMedGoogle Scholar
  21. Mahakkanukrauh P, Somsarp V (2002) Dual innervation of the brachialis muscle. Clin Anat 15:206–209PubMedCrossRefGoogle Scholar
  22. Mattei B, Schmied A, Vedel JP (2003) Recurrent inhibition of wrist extensor motoneurones: a single unit study on a deafferented patient. J Physiol 549:975–984PubMedCrossRefGoogle Scholar
  23. Matthews PB (1996) Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J Physiol 492(Pt 2):597–628PubMedGoogle Scholar
  24. Miles TS, Le TH, Turker KS (1989) Biphasic inhibitory responses and their IPSPs evoked by tibial nerve stimulation in human soleus motor neurones. Exp Brain Res 77:637–645PubMedGoogle Scholar
  25. Moritz CT, Barry BK, Pascoe MA, Enoka RM (2005) Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93:2449–2459PubMedCrossRefGoogle Scholar
  26. Murray WM, Delp SL, Buchanan TS (1995) Variation of muscle moment arms with elbow and forearm position. J Biomech 28:513–525PubMedCrossRefGoogle Scholar
  27. Nafati G, Schmied A, Rossi-Durand C (2005) Changes in the inhibitory control exerted by the antagonist Ia afferents on human wrist extensor motor units during an attention-demanding motor task. J Neurophysiol 93:2350–2353PubMedCrossRefGoogle Scholar
  28. Naito A (2004) Electrophysiological studies of muscles in the human upper limb: the biceps brachii. Anat Sci Int 79:11–20PubMedCrossRefGoogle Scholar
  29. Naito A, Shindo M, Miyasaka T, Sun YJ, Morita H (1996) Inhibitory projection from brachioradialis to biceps brachii motoneurones in human. Exp Brain Res 111:483–486PubMedCrossRefGoogle Scholar
  30. Pascoe MA, Barry BK, Riley ZA, Enoka RM (2006) Identifying the source of radial nerve afferents that inhibit biceps brachii. Med Sci Sports Exerc 38:S372Google Scholar
  31. Pierrot-Deseilligny E, Burke D (2005) The circuitry of the human spinal cord: Its role in motor control and movement disorders. Cambridge University Press, New YorkGoogle Scholar
  32. Priori A, Berardelli A, Inghilleri M, Pedace F, Giovannelli M, Manfredi M (1998) Electrical stimulation over muscle tendons in humans. Evidence favouring presynaptic inhibition of Ia fibres due to the activation of group III tendon afferents. Brain 121(Pt 2):373–380PubMedCrossRefGoogle Scholar
  33. Riley ZA, Barry BK, Pascoe MA, Enoka RM (2006) Forearm posture and reflex inhibition from brachioradialis onto motor units in biceps brachii. Soc Neurosci Abstr #656.3Google Scholar
  34. Shemmell J, Forner M, Tresilian JR, Riek S, Barry BK, Carson RG (2005) Neuromuscular adaptation during skill acquisition on a two degree-of-freedom target-acquisition task: isometric torque production. J Neurophysiol 94:3046–3057PubMedCrossRefGoogle Scholar
  35. Stephens JA, Usherwood TP, Garnett R (1976) Technique for studying synaptic connections of single motoneurones in man. Nature 263:343–344PubMedCrossRefGoogle Scholar
  36. ter Haar Romeny BM, Denier van der Gon JJ, Gielen CC (1982) Changes in recruitment order of motor units in the human biceps muscle. Exp Neurol 78:360–368Google Scholar
  37. ter Haar Romeny BM, van der Gon JJ, Gielen CC (1984) Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks. Exp Neurol 85:631–650PubMedCrossRefGoogle Scholar
  38. Turker KS, Powers RK (1999) Effects of large excitatory and inhibitory inputs on motoneuron discharge rate and probability. J Neurophysiol 82:829–840PubMedGoogle Scholar
  39. Turker KS, Powers RK (2003) Estimation of postsynaptic potentials in rat hypoglossal motoneurones: insights for human work. J Physiol 551:419–431PubMedCrossRefGoogle Scholar
  40. Turker KS, Powers RK (2005) Black box revisited: a technique for estimating postsynaptic potentials in neurons. Trends Neurosci 28:379–386PubMedCrossRefGoogle Scholar
  41. van Zuylen EJ, Gielen CC, Denier van der Gon JJ (1988) Coordination and inhomogeneous activation of human arm muscles during isometric torques. J Neurophysiol 60:1523–1548Google Scholar
  42. Vicente DP, Calvet PF, Burgaya AC, Perez ML (2005) Innervation of biceps brachii and brachialis: anatomical and surgical approach. Clin Anat 18:186–194CrossRefGoogle Scholar
  43. Windhorst U, Hamm TM, Stuart DG (1989) On the function of muscle and reflex partitioning. Behav Brain Sci 12:629–681CrossRefGoogle Scholar
  44. Zhang L, Butler J, Nishida T, Nuber G, Huang H, Rymer WZ (1998) In vivo determination of the direction of rotation and moment-angle relationship of individual elbow muscles. J Biomech Eng 120:625–633PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Benjamin K. Barry
    • 1
    • 2
    Email author
  • Zachary A. Riley
    • 1
  • Michael A. Pascoe
    • 1
  • Roger M. Enoka
    • 1
  1. 1.Department of Integrative PhysiologyUniversity of ColoradoBoulderUSA
  2. 2.School of Medical SciencesThe University of New South WalesSydneyAustralia

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