Skip to main content

Advertisement

Log in

Stretch reflexes and joint dynamics in rheumatoid arthritis

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

Abstract

In clinically diagnosed rheumatoid arthritis (RA), studies were conducted to investigate the reflex and passive tissue contribution to measured increases in joint stiffness in the resting upper limb and during constant contractions of an attached muscle. The tonic stretch reflex was induced by a servo-controlled sinusoidal stretch perturbation of the metacarpophalangeal joint of RA patients, and age- and sex-matched controls. The resulting reflexes and mechanical changes in the RA affected joint were explored. Surface electromyographic (EMG) measurements were obtained from first dorsal interosseus muscle. Reflex gain (EMG/joint angle amplitude ratio), phase difference (reflex delay after stretch), coherence square (proportion of EMG variance accounted for by joint angle changes), joint mechanical gain (torque–joint angle amplitude ratio) and mechanical phase difference (torque response delay after stretch) were determined. RA patients showed decreased reflex gain that was partly due to coexistent severe muscle weakness, as determined from maximum voluntary contraction and grip pressure estimates. The decreased reflex gain was most evident at high stretch frequency suggesting a disproportionate loss of the large diameter afferent response and also increased reflex delay in the patients. These changes ensemble suggest significant loss of neural drive to the motor unit population. Patients also showed increased joint stiffness (measured as torque gain) in the contracting muscle, but there was no evidence of reflex activity or increased stiffness at rest. This suggests that the increased joint stiffness in RA was due to changes in the mechanical properties of the active muscle–joint system rather than changes in reflex properties.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

RA:

Rheumatoid arthritis

OJS:

Objective joint stiffness

PJS:

Perceived joint stiffness

FDI:

First dorsal interosseous

MCP:

Metacarpophalangeal joint

TSR:

Tonic stretch reflex

SR:

Stretch reflex

RF:

Resonant frequency

EMG:

Electromyogram

MVC:

Maximum voluntary contraction

References

  • Agrawal V, Husain N, Das SK, Bagchi M (2003) Muscle involvement in rheumatoid arthritis: clinical and histological characteristics and review of literature. J Indian Rheumatol Assoc 11:98–103

    Google Scholar 

  • Akazawa K, Milner TE, Stein RB (1983) Modulation of reflex EMG and stiffness in response to stretch of human finger muscle. J Neurophysiol 49:16–27

    CAS  PubMed  Google Scholar 

  • Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healy LA, Kaplan SR (1988) The American rheumatism association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31:315–324

    Article  CAS  PubMed  Google Scholar 

  • Backlund L, Tiselius P (1967) Objective measurement of joint stiffness in rheumatoid arthritis. Acta Rheumatol Scand 13:275–288

    CAS  PubMed  Google Scholar 

  • Bawa P, Stein RB (1976) Frequency response of human soleus muscle. J Neurophysiol 39:788–793

    CAS  PubMed  Google Scholar 

  • Bendat JS, Piersol AG (2000) Random data: analysis and measurement procedures. Wiley, New York

    Google Scholar 

  • Brown TIH, Rack PMH, Ross HF (1982) Electromyographic responses to imposed sinusoidal movement of the human thumb. J Physiol 332:87–99

    CAS  PubMed  Google Scholar 

  • Burke D, Andrews CJ, Gillies JD (1971) The reflex response to sinusoidal stretching in spastic man. Brain 94:455–470

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cannon SC, Zahalak GI (1982) The mechanical behaviour of active human muscle in small oscillations. J Biomech 15:111–121

    Article  CAS  PubMed  Google Scholar 

  • Cathers I, O’Dwyer N, Neilson P (1999) Dependence of stretch reflexes on amplitude and bandwidth of stretch in human wrist muscle. Exp Brain Res 129:278–287

    Article  CAS  PubMed  Google Scholar 

  • Cathers I, O’Dwyer N, Neilson P (2004) Variation of magnitude and timing of wrist flexor stretch reflex across the full range of voluntary activation. Exp Brain Res 157:324–335

    Article  CAS  PubMed  Google Scholar 

  • Deseilligny EP, Burke D (2005) The circuitry of the human spinal cord. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Haigh RC, McCabe CS, Halligan PW, Blake DR (2003) Joint stiffness in a phantom limb: evidence of central nervous system involvement in rheumatoid arthritis. Rheumatology (Oxford) 42:888–892

    Article  CAS  Google Scholar 

  • Harrison B, Symmons D, Barret C, Silman A (1998) The performance of the 1987 ARA classification criteria for rheumatoid arthritis in a population based control of patients with early inflammatory arthritis. J Rheumatol 25:2320–2324

    Google Scholar 

  • Helliwell PS (1994) Normal vibration perception thresholds in rheumatoid arthritis—evidence against the neurogenic theory of articular stiffness. Clin Rheumatol 13:51–53

    Article  CAS  PubMed  Google Scholar 

  • Helliwell PS (1997) Use of an objective measure of articular stiffness to record changes in finger joints after intra-articular injection of corticosteroid. Ann Rheum Dis 56:71–73

    Article  CAS  PubMed  Google Scholar 

  • Helliwell PS, Howe A, Wright V (1988) Lack of objective evidence of stiffness in rheumatoid arthritis. Ann Rheum Dis 47:754–758

    Article  CAS  PubMed  Google Scholar 

  • Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82:2271–2283

    CAS  PubMed  Google Scholar 

  • Huxley HE (1969) The mechanism of muscle contraction. Science 164:1356–1366

    Article  CAS  PubMed  Google Scholar 

  • Inbar G, Madrid J, Rudomin P (1979) The influence of the gamma system on cross-correlated activity of Ia muscle spindles and its relation to information transmission. Neurosci Lett 13:73–78

    Article  CAS  PubMed  Google Scholar 

  • Joyce GC, Rack PMH, Ross HF (1974) The forces generated at the human elbow joint in response to imposed sinusoidal movements of the forearm. J Physiol 240:351–374

    CAS  PubMed  Google Scholar 

  • Kearney RE, Hunter IW (1982) Dynamics of human ankle stiffness: variation with displacement amplitude. J Biomech 15:753–756

    Article  CAS  PubMed  Google Scholar 

  • Kearney RE, Stein RB, Parameswaran L (1997) Identification of intrinsic and reflex contributions to human ankle stiffness dynamics. IEEE Trans Biomed Eng 44:493–504

    Article  CAS  PubMed  Google Scholar 

  • Kellgren JH, Lawrence JS (1957) Radiological assessment of osteo-arthrosis. Ann Rheum Dis 16:494–502

    Article  CAS  PubMed  Google Scholar 

  • Kirsch RF, Kearney RE (1997) Identification of time-varying stiffness dynamics of the human ankle joint during an imposed movement. Exp Brain Res 114:71–85

    Article  CAS  PubMed  Google Scholar 

  • Kirsch RF, Kearney RE, Crago PE (1994) Dynamic stiffness measurement and the control of movement. IEEE Trans Biomed Eng 42:8–429

    Google Scholar 

  • Lakie M, Robson LG (1988) Thixotropy: the effect of stretch size in relaxed frog muscle. Exp Physiol 73:127–129

    CAS  Google Scholar 

  • Lakie M, Walsh EG, Wright GW (1984) Resonance at the wrist demonstrated by the use of a torque motor: an instrumental analysis of muscle tone in man. J Physiol 353:265–285

    CAS  PubMed  Google Scholar 

  • Lansbury J (1959) Report of a three-year study on the systemic and articular indexes in rheumatoid arthritis. Arthritis Rheum 1:505

    Article  Google Scholar 

  • Lineker S, Badley E, Charles C, Hart L, Streiner D (1999) Defining morning stiffness in rheumatoid arthritis. J Rheumatol 26:1052–1057

    CAS  PubMed  Google Scholar 

  • Macefield VG, Gandevia SC, Bigland BR-R, Gorman RB, Burke D (1993) The firing rates of human motoneurons voluntarily activated in the absence of muscle afferent feedback. J Physiol 471:429–443

    CAS  PubMed  Google Scholar 

  • Magyar E, Talerman A, Mohacsy J, Wouters HW, de Buijn WC (1977) Muscle changes in rheumatoid arthritis. Virchows Arch A Pathol Anat Histol 373:267–278

    Article  CAS  PubMed  Google Scholar 

  • Matthews PBC (1993) Interaction between short- and long-latency components of the human stretch reflex during sinusoidal stretching. J Physiol 462:503–527

    CAS  PubMed  Google Scholar 

  • Matthews PBC (1994) The simple frequency response of human stretch reflexes in which either short- or long- latency components predominate. J Physiol 481.3:777–798

    Google Scholar 

  • Matthews PBC, Stein RB (1969) The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J Physiol 200:723–743

    CAS  PubMed  Google Scholar 

  • McMahon SB, Wall PD (1984) Receptive fields of lamina I projection cells move to incorporate a nearby region of injury. Pain 19:235–247

    Article  CAS  PubMed  Google Scholar 

  • Mirbagheri MM, Barbeau H, Kearney RE (2000) Intrinsic and reflex contributions to human ankle stiffness: variation with activation level and position. Exp Brain Res 135:423–436

    Article  CAS  PubMed  Google Scholar 

  • Morgan DL (1977) Separation of active and passive components of short-range stiffness of muscle. Am J Phys Med Rehabil 232:C45–C49

    CAS  Google Scholar 

  • Neilson PD, Lance JW (eds) (1978) Reflex transmission characteristics during voluntary activity in normal man and patients with movement disorders. Karger, Basel

    Google Scholar 

  • Perreault EJ, Kirsch RF, Crago PE (2001) Effects of voluntary force generation on the elastic components of end point stiffness. Exp Brain Res 141:312–323

    Article  CAS  PubMed  Google Scholar 

  • Rack PMH, Ross HF, Thilmann AF, Walters DKW (1983) Reflex responses at the human ankle: the importance of tendon compliance. J Physiol 344:503–524

    CAS  PubMed  Google Scholar 

  • Riley J, Boulis NM (2006) Molecular mechanisms of pain: a basis for chronic pain and therapeutic approaches based on the cell and the gene. Clin Neurosurg 53:77–97

    PubMed  Google Scholar 

  • Schaible H-G, Ebersberger A, Von Banchet GS (2002) Mechanisms of pain in arthritis. Ann N Y Acad Sci 966:343–354

    Article  CAS  PubMed  Google Scholar 

  • Sinkjaer T, Hayashi R (1989) Regulation of wrist stiffness by the stretch reflex. J Biomech 22:1133–1140

    Article  CAS  PubMed  Google Scholar 

  • Sinkjaer T, Magnussen I (1994) Passive intrinsic and reflex-mediated stiffness in the ankle extensors of hemiparetic patients. Brain 117:355–363

    Article  PubMed  Google Scholar 

  • Sinkjaer T, Toft E, Andreassen S (1988) Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components. J Neurophysiol 60:1110–1121

    CAS  PubMed  Google Scholar 

  • Stiles RN, Randall JE (1967) Mechanical factors in human tremor frequency. J Appl Physiol 23:324–330

    CAS  PubMed  Google Scholar 

  • Taylor A, Ellaway PH, Durbaba R, Rawlinson S (2000) Distinctive patterns of static and dynamic gamma motor activity during locomotion in decerebrate cat. J Physiol 529:825–836

    Article  CAS  PubMed  Google Scholar 

  • Unsworth A, Yung P, Haslock I (1982) Measurement of stiffness in metacarpophalangeal joint: the arthrograph. Clin Phys Physiol Meas 3:273–281

    Article  CAS  PubMed  Google Scholar 

  • Valle MS, Casabona A, Sgarlata R, Garozzo R, Vinci M, Cioni M (2006) The pendulum test as a tool to evaluate passive knee stiffness and viscosity of patients with rheumatoid arthritis. BMC Musculoskel Disord 7:89

    Article  Google Scholar 

  • Woolacott AJ, Burne JA (2006) The tonic stretch reflex and spastic hypertonia after spinal cord injury. Exp Brain Res 174:386–396

    Article  PubMed  Google Scholar 

  • Wright V, Johns RJ (1960a) Physical factors concerned with the stiffness of normal and diseased joints. Bull Johns Hopkins Hospital 106:215–231

    CAS  Google Scholar 

  • Wright V, Johns RJ (1960b) Observations on the measurement of joint stiffness. Arthritis Rheum 3:328–340

    Article  Google Scholar 

  • Wright V, Johns RJ (1961) Quantitative and qualitative analysis of joint stiffness in normal subjects and in patients with connective tissue diseases. Ann Rheum Dis 20:36–45

    Article  CAS  PubMed  Google Scholar 

  • Zahalak GI, Pramod R (1985) Myoelectric response of the human triceps brachii to displacement-controlled oscillations of the forearm. Exp Brain Res 58:305–317

    Article  CAS  PubMed  Google Scholar 

  • Zhang L-Q, Rymer WZ (1997) Simultaneous and non-linear identification of mechanical and reflex properties of human elbow joint muscles. IEEE Trans Biomed Eng 44:1192–1209

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors are indebted to the subjects for the many hours of participation on the experimentation throughout the project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John A. Burne.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rajagopalan, A., Burne, J.A. Stretch reflexes and joint dynamics in rheumatoid arthritis. Exp Brain Res 201, 37–45 (2010). https://doi.org/10.1007/s00221-009-2010-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-2010-3

Keywords

Navigation