Skip to main content
SpringerLink
Log in

Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Previous studies have shown that deficits in agonist–antagonist muscle activation in the single-joint elbow system in patients with spastic hemiparesis are directly related to limitations in the range of regulation of the thresholds of muscle activation. We extended these findings to the double-joint, shoulder-elbow system in these patients. Ten non-disabled individuals and 11 stroke survivors with spasticity in upper limb muscles participated. Stroke survivors had sustained a single unilateral stroke 6–36 months previously, had full pain-free passive range of motion of the affected shoulder and elbow and had some voluntary control of the arm. EMG activity from four elbow and two shoulder muscles was recorded during quasi-static (<5°/s) stretching of elbow flexors/extensors and during slow voluntary elbow flexion/extension movement through full range. Stretches and active movements were initiated from full elbow flexion or extension with the shoulder in three different initial positions (60°, 90°, 145° horizontal abduction). SRTs were defined as the elbow angle at which EMG signals began to exceed 2SD of background noise. SRT angles obtained by passive muscle stretch were compared with the angles at which the respective muscles became activated during voluntary elbow movements. SRTs in elbow flexors were correlated with clinical spasticity scores. SRTs of elbow flexors and extensors were within the biomechanical range of the joint and varied with changes in the shoulder angle in all subjects with hemiparesis but could not be reached in this range in all healthy subjects when muscles were initially relaxed. In patients, limitations in the regulation of SRTs resulted in a subdivision of all-possible shoulder-elbow arm configurations into two areas, one in which spasticity was present (“spatial spasticity zone”) and another in which it was absent. Spatial spasticity zones were different for different muscles in different patients but, taken together, for all elbow muscles, the zones occupied a large part of elbow-shoulder joint space in each patient. The shape of the boundary between the spasticity and no-spasticity zones depended on the state of reflex inter-joint interaction. SRTs in single- and double-joint flexor muscles correlated with the positions at which muscles were activated during voluntary movements, for all shoulder angles, and this effect was greater in elbow flexor muscles (brachioradialis, biceps brachii). Flexor SRTs correlated with clinical spasticity in elbow flexors only when elbow muscles were at mid-length (90°). These findings support the notion that motor impairments after CNS damage are related to deficits in the specification and regulation of SRTs, resulting in the occurrence of spasticity zones in the space of elbow-shoulder configurations. It is suggested that the presence of spatial spasticity zones might be a major cause of motor impairments in general and deficits in inter-joint coordination in particular in patients with spasticity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Archambault PS, Mihaltchev P, Levin MF, Feldman AG (2005) Basic elements of arm postural control analyzed by unloading. Exp Brain Res 164:225–241

    Article  PubMed  Google Scholar 

  • Asatryan DG, Feldman AG (1965) On the functional structure of the nervous system during movement control or preservation of a stationary posture. I. Mechanographic analysis of the action of a joint during the performance of a postural task. Biofizika 10:837–846

    Google Scholar 

  • Beer RF, Dewald JPA, Rymer WZ (2000) Deficits in the coordination of multi-joint arm movements in patients with hemiparesis: evidence for disturbed control of limb dynamics. Exp Brain Res 131:305–319

    Article  PubMed  CAS  Google Scholar 

  • Bohannon RW, Larkin PA, Smith MB, Horton MG (1987) Relationship between static muscle strength deficits and spasticity in stroke patients with hemiparesis. Phys Ther 67:1068–1071

    PubMed  CAS  Google Scholar 

  • Burne JA, Carleton VL, O’Dwyer NJ (2005) The spasticity paradox: movement disorder or disorder of resting limbs? J Neurol, Neurosurg Psychiatr 76:47–54

    Article  CAS  Google Scholar 

  • Capaday C (1995) The effects of baclofen on the stretch reflex parameters of the cat. Exp Brain Res 104:287–296

    Article  PubMed  CAS  Google Scholar 

  • 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 78:465–478

    Article  PubMed  CAS  Google Scholar 

  • Cavallari P, Katz R, Penicaud A (1992) Pattern of projections of group I afferents from elbow muscles to motoneurones supplying wrist muscles in man. Exp Brain Res 91:311–319

    Article  PubMed  CAS  Google Scholar 

  • Corcos DM, Gottlieb GL, Penn RD, Myklebust B, Agarwal GC (1986) Movement deficits caused by hyperexcitable stretch reflexes in spastic humans. Brain 109:1043–1058

    Article  PubMed  Google Scholar 

  • Créange A, Faist M, Katz R, Penicaud A (1992) Distribution of heteronymous Ia facilitation and recurrent inhibition in the human deltoid motor nucleus. Exp Brain Res 90:620–624

    Article  PubMed  Google Scholar 

  • Dewald JP, Pope PS, Given JD, Buchanan TS, Rymer WZ (1995) Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects. Brain 118:495–510

    Article  PubMed  Google Scholar 

  • Fedirchuk B, Dai Y (2004) Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J Physiol 557:355–361

    Article  PubMed  CAS  Google Scholar 

  • Feldman AG (1966) Functional tuning of the nervous system with control of movment or maintenance of a steady posture: 2. Controllable parameters of the muscle. Biophysics 11:565–578

    Google Scholar 

  • Feldman AG, Orlovsky GN (1972) The influence of different descending systems on the tonic stretch reflex in the cat. Exp Neurol 37:481–494

    Article  PubMed  CAS  Google Scholar 

  • Feldman AG, Levin MF (1995) The origin and use of positional frames of reference in motor control. Beh Brain Sci 18:723–744

    Article  Google Scholar 

  • Feldman AG, Goussev V, Sangole A, Levin MF (2007) Threshold position control and the principle of minimal interaction in motor actions. Prog Brain Res (in press)

  • Fugl-Meyer AR, Jaasko L, Leyman I, Olsson S, Steglind S (1975) The post-stroke hemiplegic patient. I. A method for evaluation of physical performance. Scand J Rehab Med 7:13–31

    CAS  Google Scholar 

  • Gracies JM, Meunier S, Pierrot-Deseilligny E, Simonetta M (1991) Pattern of propriospinal-like excitation to different species of human upper limb motoneurones. J Physiol 434:151–167

    PubMed  CAS  Google Scholar 

  • Goulet C, Arsenault AB, Bourbonnais D, Laramée MT, Lepage Y (1996) Effects of transcutaneous electrical nerve stimulation on H-reflex and spinal spasticity. Scand J Rehabil Med 28:167–176

    Google Scholar 

  • Hagbarth K-E, Hagglund JV, Nordin M, Wallin EU (1987) Muscle thixotrophy and its effects on spindle and reflex responses to stretch. In: Struppler A, Weindl A (Eds) Clinical aspects of sensory motor integration. Springer, Berlin, pp 91–97

    Google Scholar 

  • Hultborn H, Meunier S, Pierrot-Deseilligny E, Shindo M (1987) Changes in presynaptic inhibition of Ia fibres at the onset of voluntary contraction in man. J Physiol 389:757–772

    PubMed  CAS  Google Scholar 

  • Hultborn H, Kiehn O (1992) Neuromodulation of vertebrate motor neuron membrane properties. Curr Opp Neurobiol 2:770–775

    Article  CAS  Google Scholar 

  • Jobin A, Levin MF (2000) Regulation of stretch reflex threshold in elbow flexors in children with cerebral palsy: a new measure of spasticity. Dev Med Child Neurol 42:531–540

    Article  PubMed  CAS  Google Scholar 

  • Katz R, Penicaud A, Rossi A (1991) Reciprocal Ia inhibition between elbow flexors and extensors in the human. J Physiol 437:269–286

    PubMed  CAS  Google Scholar 

  • Lance JW (1980) The control of muscle tone, reflexes and movement. Robert Wartenberg Lecture. Neurol 30:309–326

    Google Scholar 

  • Lee WA, Boughton A, Rymer WZ (1987) Absence of stretch gain enhancement in voluntarily activated spastic muscle. Exp Neurol 98:317–335

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Dimov M (1997) Spatial zones for muscle coactivation and the control of postural stability. Brain Res 757:43–59

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Feldman AG (1994) The role of stretch reflex threshold regulation in normal and impaired motor control. Brain Res 657:23–30

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Hui-Chan CWY (1992) Relief of hemiparetic spasticity by TENS is associated with improvement in reflex and voluntary motor functions. Electroenceph Clin Neurophysiol 85:131–142

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Selles RW, Verheul MHG, Meijer OG (2000) Deficits in the coordination of agonist and antagonist muscles in stroke patients: implications for normal motor control. Brain Res 853:352–369

    Article  PubMed  CAS  Google Scholar 

  • Lundberg A (1967) The supraspinal control of transmission in spinal reflex pathways. Electroenceph Clin Neurophysiol Suppl 25:35–46

    Google Scholar 

  • Marchand-Pauvert V, Nicolas G, Pierrot-Deseilligny E (2000) Monosynaptic Ia projections from intrinsic hand muscles to forearm motoneurones in humans. J Physiol 525:241–252

    Article  PubMed  CAS  Google Scholar 

  • Matthews PBC (1959) The dependence of tension upon extension the stretch reflex of the soleus muscles of the decerebrate cat. J Physiol (Lond) 147:521–546

    CAS  Google Scholar 

  • Mazevet D, Meunier S, Pradat-Diehl P, Marchand-Pauvert V, Pierrot-Deseilligny E (2003) changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. Brain 126:988–1000

    Article  PubMed  Google Scholar 

  • McClelland VM, Miller S, Eyre JA (2001) Short latency heteronymous excitatory and inhibitory reflexes between antagonist and heteronymous muscles of the human shoulder and upper limb. Brain Res 299:82–93

    Article  Google Scholar 

  • Meunier S, Pierrot-Deseilligny E (1998) Cortical control of presynaptic inhibition of Ia afferents in humans. Exp Brain Res 119:415–426

    Article  PubMed  CAS  Google Scholar 

  • Michaelsen SM, Luta A, Roby-Brami A, Levin MF (2001) Effect of trunk restraint on the recovery of reaching movements in hemiparetic patients. Stroke 32:1875–1883

    PubMed  CAS  Google Scholar 

  • Mihaltchev P, Archambault PS, Feldman AG, Levin MF (2005) Control of double-joint arm posture in adults with unilateral brain damage. Exp Brain Res 163:468–486

    Article  PubMed  CAS  Google Scholar 

  • Musampa KN, Mathieu P, Levin MF (2005) Relation between stretch reflex thresholds and abnormal co-contraction in the arm of patients with spastic hemiparesis. Progress in Motor Control V. Penn State University, August 2005. Abstract

  • Nadeau S, Arsenault AB, Gravel D, Lepage Y, Bourbonnais D (1998) Analysis of the spasticity index used in adults with a stroke. Can J Rehabil 11:219–220

    Google Scholar 

  • Nichols TR (1989) The organization of heterogenic reflexes among muscles crossing the ankle joint in the decerebrate cat. J Physiol 410:463–477

    PubMed  CAS  Google Scholar 

  • O´Dwyer NJ, Ada L, Neilson PD (1996) Spasticity and muscle contracture following stroke. Brain 119:1737–1749

    Article  Google Scholar 

  • Pigeon P, Yahia L, Feldman AG (1996) Moment arms and lengths of human upper limb muscles as functions of joint angles. J Biomech 29:1365–1370

    Article  PubMed  CAS  Google Scholar 

  • Powers RK, Marder-Meyer J, Rymer WZ (1988) Quantitative relations between hypertonia and stretch reflex threshold in spastic hemiparesis. Ann Neurol 23:115–124

    Article  PubMed  CAS  Google Scholar 

  • Powers RK, Campbell DL, Rymer WZ (1989) Stretch reflex dynamics in spastic elbow flexor muscles. Ann Neurol 25:32–42

    Article  PubMed  CAS  Google Scholar 

  • Roby-Brami A, Fuchs S, Mokhtari M, Bussel B (1997) Reaching and grasping strategies in hemiparetic patients. Motor Control 1:72–91

    Google Scholar 

  • Sahrmann SA, Norton BJ (1977) The relationship of voluntary movement to spasticity in the upper motor neuron syndrome. Ann Neurol 2:460–465

    Article  PubMed  CAS  Google Scholar 

  • Schmit BD, Dewald JP, Rymer WZ (2000) Stretch reflex adaptation in elbow flexors during repeated passive movements in unilateral brain-injured patients. Arch Phys Med Rehabil 81:269–278

    Article  PubMed  CAS  Google Scholar 

  • Ter Haar Romeny BM, Denier van der Gon JJ, Gielen CCCAM (1984) Relation between location of a motor unit in the human biceps brachii and its critical firing levels for different tasks. Exp Neurol 85:631–650

    Article  PubMed  CAS  Google Scholar 

  • Thilmann AF, Fellows SJ, Garms E (1991) The mechanism of spastic muscle hypertonus. Variation in reflex gain over the time course of spasticity. Brain 114:233–244

    PubMed  Google Scholar 

  • Van Zuylen EJ, Gielen CCAM, Denier Van Der Gon JJ (1988) Coordination and inhomogeneous activation of human arm msucles during isometric troques. J Neurophysiol 60:1523–1548

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to express their sincere gratitude to all the patients who participated voluntarily in this study. We also acknowledge the contribution of Anatol Feldman in the preparation of the manuscript. This project was supported by NSERC and the Physiotherapy Foundation of Canada. NKM was a grantee of CIHR-MENTOR Training Program.

Author information

Authors and Affiliations

  1. School of Rehabilitation, University of Montreal, Montreal, QC, Canada

    Nadine K. Musampa

  2. Department of Physiology, University of Montreal, Montreal, QC, Canada

    Pierre A. Mathieu

  3. Physical Therapy Program, School of Physical and Occupational Therapy, McGill University, 3654 Promenade Sir William Osler, H3G 1Y5, Montreal, QC, Canada

    Mindy F. Levin

  4. Centre for Interdisciplinary Research in Rehabilitation (CRIR), Montreal, Canada

    Nadine K. Musampa, Pierre A. Mathieu & Mindy F. Levin

Authors
  1. Nadine K. Musampa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pierre A. Mathieu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mindy F. Levin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mindy F. Levin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Musampa, N.K., Mathieu, P.A. & Levin, M.F. Relationship between stretch reflex thresholds and voluntary arm muscle activation in patients with spasticity. Exp Brain Res 181, 579–593 (2007). https://doi.org/10.1007/s00221-007-0956-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-007-0956-6

Keywords

Search

Navigation