Abstract
The operational definition of spasticity is focused on increased resistance of joints to passive rotation and the possible origin of this increased resistance in the induced tonic stretch reflex (TSR). This term is applied in the context of both cerebral and spinal injury, implying that a similar reflex mechanism underlies the two disorders. From recent studies it is clear that increased passive joint resistance in resting limbs following stroke is highly correlated with the induced TSR, but this evidence is lacking in spinal injury. The contribution of the TSR to hypertonia in spinal cord injury (SCI) is unclear and it is possible that hypertonia has a different origin in SCI. The contribution of resting and activated TSR activity to joint stiffness was compared in SCI and normal subjects. The magnitude of the TSR in ankle dorsiflexors (DF) and plantarflexors (PF) and mechanical ankle resistive torque were measured at rest and over a range of contraction levels in normal subjects. Similar measures were made in 13 subjects with SCI to the limits of their range of voluntary contraction. Normals and SCI received a pseudo-sinusoidal stretch perturbation of maximum amplitude ± 20° and frequency band 0.1–3.5 Hz that was comparable to that used in manual clinical testing of muscle tone. Elastic resistance and resonant frequency of the ankle joint, after normalization for limb volume, were significantly lower in complete and incomplete SCI than normal subjects. No reflex response related to stretch velocity was observed. Resting DF and PF TSR gain, when averaged over the tested band of frequencies, were significantly lower in complete SCI than in resting normal subjects (<0.5 μV/deg). Linear regression analysis found no significant relationship between TSR gain and resting joint stiffness in SCI. Mean TSR gain of DFs and PFs at rest was not correlated with the subject variables: age, time since SCI, level of injury, Frankel score, number of spasms per day, Ashworth score or anti-spastic medication. DF and PF reflex gain were linearly related to voluntary contraction level and regression analysis produced similar slopes in incomplete SCI and normal subjects. Hence TSR loop gain was not significantly increased in SCI at any equivalent contraction level. Extrapolation of the regression lines to zero contraction level predicted that reflex threshold was not reduced in SCI. Low frequency passive stretches did not induce significant TSR activity in the resting limbs of any member of this SCI group. The TSR thus did not contribute to their clinical hypertonia. Other reflex mechanisms must contribute to hypertonia as assessed clinically. This result contrasts with our similar study of cerebral spasticity after stroke, where a comparable low frequency stretch perturbation produced clear evidence of increased TSR gain that was correlated with the hypertonia at rest. We conclude that a low frequency stretch perturbation clearly distinguished between spasticity after stroke and SCI. Spasticity in the two conditions is not equivalent and care should be taken in generalizing results between them.
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Notes
Just over 50% of complete patients were medicated. This mix should have been optimal to show a significant difference between medicated and un-medicated completes with respect to the main test parameters, reflex activity and biomechanical joint stiffness. No such difference was found. Further, three of four incompletes were medicated, yet their reflex activity and biomechanical stiffness were significantly higher than completes. There was thus no evidence that medication was a major factor in reducing reflex activity or biomechanical stiffness.
Abbreviations
- DF:
-
Dorsiflexor
- PF:
-
Plantarflexor
- EMG:
-
Electromyogram
- MVC:
-
Maximum voluntary contraction
- RF:
-
Resonant frequency
- SCI:
-
Spinal cord injury
- TSR:
-
Tonic stretch reflex
References
Bach TM, Chapman AE, Calvert TW (1983) Mechanical resonance of the human body during voluntary oscillations about the ankle joint. J Biomechanics 16:85–90
Bendat JS, Piersol AG (1971) Random data: analysis and measurement procedures. Wiley, New York
Bohannon RW, Smith MB (1987) Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 67:206–207
Burne JA, Lippold OC (1996) Reflex inhibition following electrical stimulation over muscle tendons in man. Brain 119:1107–1114
Burne JA, Carleton V, O’Dwyer N (2005) The spasticity paradox: movement disorder or disorder of resting limbs? J Neurol Neurosurg Psychiatr 76:47–54
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
Dimitrijevic MR, Nathan PW (1967) Studies of spasticity in man2. Analysis of stretch reflexes in spasticity. Brain 90:333–358
Douglas AJ, Walsh EG, Wright GW, Edmond P (1989) Muscle tone around the human knee in paraplegia. Quart J Exp Physiol 74:897–905
Faist M, Mazevet D, Dietz V, Pierrot-Deseilligny E (1994) A quantitative assessment of presynaptic inhibition of Ia afferents in spastics: differences in hemiplegics and paraplegics. Brain 117:1449–1455
Faist M, Ertel M, Berger W, Dietz V (1999) Impaired modulation of quadriceps tendon jerk reflex during spastic gait: differences between spinal and cerebral lesions. Brain 122:567–579
Frankel HL, Hancock DD, Hyslop G, Melzak J, Michaelis LS, Ungar GH, Vernon JD (1969) The value of postural reduction in initial management of closed injuries of the spine with paraplegia and tetraplegia. I. Paraplegia 7:179–192
Gildenberg PL, Campos RJ, Dimitrijevic MR (1985) Characteristics of the tonic stretch reflex in spastic spinal cord and head-injured patients. Appl Neurophysiol 48:106–110
Given JD, Dewald JPA, Rymer WZ (1995) Joint dependent passive stiffness in paretic and contralateral limbs of spastic patients with hemiparetic stroke. J Neurol Neurosurg Psychiatr 59:271–279
Gottlieb GL, Agarwal GC (1977) Oscillation of the human ankle joint in response to applied sinusoidal torque of the foot. J Physiol (Lond) 266:151–176
Gottlieb GL, Agarwal GC (1978) Dependence of human ankle compliance on joint angle. J Biomech 11:177–181
Hiersemenzel L-P, Curt A, Deitz V (2000) From spinal shock to spasticity: Neuronal adaptations to a spinal cord injury. Neurology 54:1574–1582
Hunter IW, Kearney RE (1982a) Dynamics of human ankle stiffness. Variation with mean ankle torques. J Biomech 15:747–752
Hunter IW, Kearney RE (1982b) Dynamics of human ankle stiffness. Variation with displacement amplitude. J Biomech 15:753–756
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 (Lond) 240:351–374
Ko HY, Ditunno JF, Graziani V, Little JW (1999) The pattern of reflex recovery during spinal shock. Spinal Cord 37:402–409
Kovanen V, Suominen H, Heikkinen E (1984) Collagen of slow twitch and fast twitch muscle fibres in different types of rat skeletal muscle. Eur J Appl Physiol 52:235–232
Lance JW (1980) Pathophysiology of spasticity and clinical experience with baclofen. In: Feldman RG, Young RR, Koella WP (eds) Spasticity: disordered motor control. Year Book Publishers, Chicago
Mathews PBC (1994) The simple frequency response of human stretch reflexes in which either short- or long-latency components predominate. J Physiol 481:777–798
Matthews PBC (1981) Muscle spindles, their messages and their fusimotor supply. In: Brookhart J, Mountcastle VB (eds) The nervous system, vol II. Motor control, part 1. American Physiological Society, Bethesda, pp 189–228
Mense S, Meyer H (1985) Different types of slowly conducting afferent units in cat skeletal muscle and tendon. J Physiol 363:403–417
Mirbagheri MM, Barbeau H, Ladouceur M, Kearney RE (2001) Intrinsic and reflex stiffness in normal and spastic, spinal cord injured subjects. Exp Brain Res 141:446–459
O’Dwyer ND, Neilson PD, Nash J (1989) Mechanisms of muscle growth related to muscle contracture in cerebral palsy. Dev Med Child Neurol 31:543–547
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 121:373–380
Schmit BD, Benz EN (2002) Extensor reflexes in human spinal cord injury: activation by hip proprioceptors. Exp Brain Res 145:520–527
Schmit BD, McKenna-Cole A, Rymer WZ (2000) Flexor reflexes in spinal cord injury triggered by imposed ankle rotation. Muscle Nerve 23:793–803
Schmit BD, Benz EN, Rymer WZ (2002a) Afferent mechanisms for the reflex response to imposed ankle movement in chronic spinal cord injury. Exp Brain Res 145:40–49
Schmit BD, Benz EN, Rymer WZ (2002b) Reflex mechanisms for motor impairment in spinal cord injury. Adv Exp Med Biol 508:315–323
Schomburg ED, Steffens H, Kniffki KD (1999) Contribution of group III and IV muscle afferents to multisensorial spinal motor control in cats. Neurosci Res Suppl 33:195–206
Shahani BT, Young RR (1971) Human flexor reflexes. J Neurol Neurosurg Psychiatr 34:616–627
Toft E, Sinkjaer T, Andreassen S (1989) Mechanical and electromyographic responses to stretch of the human anterior tibial muscle at different levels of contraction. Exp Brain Res 74:213–219
Toft E, Sinkjaer T, Andreassen S, Larsen K (1991) Mechanical and electromyographic responses to stretch of the human ankle extensors. J Neurophysiol 65:1402–1410
Tsementzis SA, Gillingham FJ, Gordon A, Lakie MD (1980) Two methods of measuring muscle tone applied in patients with decerebrate rigidity. J Neurol Neurosurg Psychiatr 43:25–36
Valbo AB (1970) Discharge patterns in human muscle spindle afferents during isometric voluntary contractions. Acta Physiol Scand 80:552–566
Walsh EG, Wright GW, Brown K, Bell E (1990a) Biodynamics of the ankle in spastic children- Effect of chronic stretching of the calf musculature. Exp Physiol 75:423–425
Walsh EG, Brown K, Wright GW (1990b) Resonant frequency of the ankle in juvenile hemiplegia (abstract). Proc Physiol Soc 31P
Zhang L, Rymer WZ (1997) Simultaneous and nonlinear identification of mechanical and reflex properties of human elbow joint muscles. IEEE Trans Biomed Eng 44:1192–1209
Acknowledgements
The authors are grateful to the Director of Clinical Services at the Royal Rehabilitation Centre Sydney, Dr Sue Rutkowski, her staff and patients for their assistance and support during data collection.
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Woolacott, A.J., Burne, J.A. The tonic stretch reflex and spastic hypertonia after spinal cord injury. Exp Brain Res 174, 386–396 (2006). https://doi.org/10.1007/s00221-006-0478-7
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DOI: https://doi.org/10.1007/s00221-006-0478-7