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Published in: Experimental Brain Research 1-2/2010

01-11-2010 | Research Article

Co-contraction modifies the stretch reflex elicited in muscles shortened by a joint perturbation

Authors: Gwyn N. Lewis, Colum D. MacKinnon, Randy Trumbower, Eric J. Perreault

Published in: Experimental Brain Research | Issue 1-2/2010

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Abstract

Simultaneous contraction of agonist and antagonist muscles acting about a joint influences joint stiffness and stability. Although several studies have shown that reflexes in the muscle lengthened by a joint perturbation are modulated during co-contraction, little attention has been given to reflex regulation in the antagonist (shortened) muscle. The goal of the present study was to determine whether co-contraction gives rise to altered reflex regulation across the joint by examining reflexes in the muscle shortened by a joint perturbation. Reflexes were recorded from electromyographic activity in elbow flexors and extensors while positional perturbations to the elbow joint were applied. Perturbations were delivered during isolated activation of the flexor or extensor muscles as well as during flexor and extensor co-contraction. Across the group, the shortening reflex in the elbow extensor switched from suppression during isolated extensor muscle activation to facilitation during co-contraction. The shortening reflex in the elbow flexor remained suppressive during co-contraction but was significantly smaller compared to the response obtained during isolated elbow flexor activation. This response in the shortened muscle was graded by the level of activation in the lengthened muscle. The lengthening reflex did not change during co-contraction. These results support the idea that reflexes are regulated across multiple muscles around a joint. We speculate that the facilitatory response in the shortened muscle arises through a fast-conducting oligosynaptic pathway involving Ib interneurons.
Literature
go back to reference Akazawa K, Milner TE, Stein RB (1983) Modulation of reflex EMG and stiffness in response to stretch of human finger muscle. J Neurophysiol 49:16–27PubMed Akazawa K, Milner TE, Stein RB (1983) Modulation of reflex EMG and stiffness in response to stretch of human finger muscle. J Neurophysiol 49:16–27PubMed
go back to reference Angel RW, Lewitt PA (1978) Unloading and shortening reactions in Parkinson’s disease. J Neurol Neurosurg Psychiatry 41:919–923CrossRefPubMed Angel RW, Lewitt PA (1978) Unloading and shortening reactions in Parkinson’s disease. J Neurol Neurosurg Psychiatry 41:919–923CrossRefPubMed
go back to reference Bawa P, Sinkjaer T (1999) Reduced short and long latency reflexes during voluntary tracking movement of the human wrist joint. Acta Physiol Scand 167:241–246CrossRefPubMed Bawa P, Sinkjaer T (1999) Reduced short and long latency reflexes during voluntary tracking movement of the human wrist joint. Acta Physiol Scand 167:241–246CrossRefPubMed
go back to reference Berardelli A, Hallett M (1984) The shortening reaction of human tibialis anterior. Neurology 34:242–246PubMed Berardelli A, Hallett M (1984) The shortening reaction of human tibialis anterior. Neurology 34:242–246PubMed
go back to reference Carter RR, Crago PE, Gorman PH (1993) Nonlinear stretch reflex interaction during cocontraction. J Neurophysiol 69:943–952PubMed Carter RR, Crago PE, Gorman PH (1993) Nonlinear stretch reflex interaction during cocontraction. J Neurophysiol 69:943–952PubMed
go back to reference Colebatch JG, Gandevia SC, McCloskey DI, Potter EK (1979) Subject instruction and long-latency reflex responses to muscle stretch. J Physiol 292:527–534PubMed Colebatch JG, Gandevia SC, McCloskey DI, Potter EK (1979) Subject instruction and long-latency reflex responses to muscle stretch. J Physiol 292:527–534PubMed
go back to reference Crago PE, Houk JC, Hasan Z (1976) Regulatory actions of human stretch reflex. J Neurophysiol 39:925–935PubMed Crago PE, Houk JC, Hasan Z (1976) Regulatory actions of human stretch reflex. J Neurophysiol 39:925–935PubMed
go back to reference Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB (2003) Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 126:495–507CrossRefPubMed Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB (2003) Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 126:495–507CrossRefPubMed
go back to reference Day SJ, Hulliger M (2001) Experimental simulation of cat electromyogram: evidence for algebraic summation of motor-unit action-potential trains. J Neurophysiol 86:2144–2158PubMed Day SJ, Hulliger M (2001) Experimental simulation of cat electromyogram: evidence for algebraic summation of motor-unit action-potential trains. J Neurophysiol 86:2144–2158PubMed
go back to reference Dietz V, Bischer M, Faist M, Trippel M (1990) Amplitude modulation of the human quadriceps tendon jerk reflex during gait. Exp Brain Res 82:211–213CrossRefPubMed Dietz V, Bischer M, Faist M, Trippel M (1990) Amplitude modulation of the human quadriceps tendon jerk reflex during gait. Exp Brain Res 82:211–213CrossRefPubMed
go back to reference Dietz V, Discher M, Trippel M (1994) Task-dependent modulation of short- and long-latency electromyographic responses in upper limb muscles. Electroencephalogr Clin Neurophysiol 93:49–56CrossRefPubMed Dietz V, Discher M, Trippel M (1994) Task-dependent modulation of short- and long-latency electromyographic responses in upper limb muscles. Electroencephalogr Clin Neurophysiol 93:49–56CrossRefPubMed
go back to reference Doemges F, Rack PM (1992) Task-dependent changes in the response of human wrist joints to mechanical disturbance. J Physiol 447:575–585PubMed Doemges F, Rack PM (1992) Task-dependent changes in the response of human wrist joints to mechanical disturbance. J Physiol 447:575–585PubMed
go back to reference Enoka RM (1997) Neural strategies in the control of muscle force. Muscle Nerve S5:66–69CrossRef Enoka RM (1997) Neural strategies in the control of muscle force. Muscle Nerve S5:66–69CrossRef
go back to reference Enriquez-Denton M, Nielsen JB, Perreault MC, Morita H, Petersen N, Hultborn H (2000) Presynaptic control of transmission along the pathway mediating disynaptic reciprocal inhibition in the cat. J Physiol 526:623–637CrossRefPubMed Enriquez-Denton M, Nielsen JB, Perreault MC, Morita H, Petersen N, Hultborn H (2000) Presynaptic control of transmission along the pathway mediating disynaptic reciprocal inhibition in the cat. J Physiol 526:623–637CrossRefPubMed
go back to reference Gottlieb GL, Myklebust BM, Penn RD, Agarwal GC (1982) Reciprocal excitation of muscle antagonists by the primary afferent pathway. Exp Brain Res 46:454–456CrossRefPubMed Gottlieb GL, Myklebust BM, Penn RD, Agarwal GC (1982) Reciprocal excitation of muscle antagonists by the primary afferent pathway. Exp Brain Res 46:454–456CrossRefPubMed
go back to reference Hammond PH (1956) The influence of prior instruction to the subject on an apparently involuntary neuro-muscular response. Society 17P–18P Hammond PH (1956) The influence of prior instruction to the subject on an apparently involuntary neuro-muscular response. Society 17P–18P
go back to reference Hultborn H, Jankowska E, Lindstrom S (1971) Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurons. J Physiol 215:591–612PubMed Hultborn H, Jankowska E, Lindstrom S (1971) Recurrent inhibition from motor axon collaterals of transmission in the Ia inhibitory pathway to motoneurons. J Physiol 215:591–612PubMed
go back to reference Hultborn H, Illert M, Santini M (1976) Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. II. Effects from segmental flexor reflex pathways. Acta Physiol Scand 96:351–367CrossRefPubMed Hultborn H, Illert M, Santini M (1976) Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. II. Effects from segmental flexor reflex pathways. Acta Physiol Scand 96:351–367CrossRefPubMed
go back to reference Humphrey DR (1982) Separate cell systems in the motor cortex of the monkey for the control of joint movement and of joint stiffness. Electroencephalogr Clin Neurophysiol 36:393–408 Humphrey DR (1982) Separate cell systems in the motor cortex of the monkey for the control of joint movement and of joint stiffness. Electroencephalogr Clin Neurophysiol 36:393–408
go back to reference Humphrey DR, Reed DJ (1983) Separate cortical systems for control of joint movement and joint stiffness: reciprocal activation and coactivation of antagonist muscles. Adv Neurol 39:347–372PubMed Humphrey DR, Reed DJ (1983) Separate cortical systems for control of joint movement and joint stiffness: reciprocal activation and coactivation of antagonist muscles. Adv Neurol 39:347–372PubMed
go back to reference Jankowska E, Padel Y, Tanaka R (1976) Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey. J Physiol 258:467–487PubMed Jankowska E, Padel Y, Tanaka R (1976) Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey. J Physiol 258:467–487PubMed
go back to reference Jankowska E, Johannisson T, Lipski J (1981) Common interneurones in reflex pathways from group 1a and 1b afferents of ankle extensors in the cat. J Physiol 310:381–402PubMed Jankowska E, Johannisson T, Lipski J (1981) Common interneurones in reflex pathways from group 1a and 1b afferents of ankle extensors in the cat. J Physiol 310:381–402PubMed
go back to reference Johannsen P, Christensen LOD, Sinkjaer T, Nielsen JB (2001) Cerebral functional anatomy of voluntary contractions of ankle muscles in man. J Physiol 535:397–406CrossRefPubMed Johannsen P, Christensen LOD, Sinkjaer T, Nielsen JB (2001) Cerebral functional anatomy of voluntary contractions of ankle muscles in man. J Physiol 535:397–406CrossRefPubMed
go back to reference Katz R, Penicaud A, Rossi A (1991) Reciprocal Ia inhibition between elbow flexors and extensors in the human. J Physiol 437:269–286PubMed Katz R, Penicaud A, Rossi A (1991) Reciprocal Ia inhibition between elbow flexors and extensors in the human. J Physiol 437:269–286PubMed
go back to reference Kornecki S (1992) Mechanism of muscular stabilization process in joints. J Biomech 25:235245CrossRef Kornecki S (1992) Mechanism of muscular stabilization process in joints. J Biomech 25:235245CrossRef
go back to reference Krutky MA, Ravichandran VJ, Trumbower RD, Perreault EJ (2010) Interactions between limb and environmental mechanics influence stretch reflex sensitivity in the human arm. J Neurophysiol 103:429–440CrossRefPubMed Krutky MA, Ravichandran VJ, Trumbower RD, Perreault EJ (2010) Interactions between limb and environmental mechanics influence stretch reflex sensitivity in the human arm. J Neurophysiol 103:429–440CrossRefPubMed
go back to reference Lacquaniti F, Borghese NA, Carrozzo M (1991) Transient reversal of the stretch reflex in human arm muscles. J Neurophysiol 66:939–954PubMed Lacquaniti F, Borghese NA, Carrozzo M (1991) Transient reversal of the stretch reflex in human arm muscles. J Neurophysiol 66:939–954PubMed
go back to reference Lance JW, Degail P (1965) Spread of phasic muscle reflexes in normal and spastic subjects. J Neurol Neurosurg Psychiatry 28:328–334CrossRefPubMed Lance JW, Degail P (1965) Spread of phasic muscle reflexes in normal and spastic subjects. J Neurol Neurosurg Psychiatry 28:328–334CrossRefPubMed
go back to reference Laporte Y, Lloyd DPC (1952) Nature and significance of the reflex connections established by large afferent fibers of muscular origin. Am J Physiol 169:609–621PubMed Laporte Y, Lloyd DPC (1952) Nature and significance of the reflex connections established by large afferent fibers of muscular origin. Am J Physiol 169:609–621PubMed
go back to reference Lewis GN, MacKinnon CD, Perreault EJ (2006) The effect of task instruction on the excitability of spinal and supraspinal reflex pathways projecting to the biceps muscle. Exp Brain Res 174:413–425CrossRefPubMed Lewis GN, MacKinnon CD, Perreault EJ (2006) The effect of task instruction on the excitability of spinal and supraspinal reflex pathways projecting to the biceps muscle. Exp Brain Res 174:413–425CrossRefPubMed
go back to reference Matthews PBC (1986) Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374:73–90PubMed Matthews PBC (1986) Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374:73–90PubMed
go back to reference Milner TE, Cloutier C (1993) Compensation for mechanically unstable loading in voluntary wrist movement. Exp Brain Res 94:522–532CrossRefPubMed Milner TE, Cloutier C (1993) Compensation for mechanically unstable loading in voluntary wrist movement. Exp Brain Res 94:522–532CrossRefPubMed
go back to reference Milner TE, Cloutier C (1998) Damping of the wrist joint during voluntary movement. Exp Brain Res 122:309–317CrossRefPubMed Milner TE, Cloutier C (1998) Damping of the wrist joint during voluntary movement. Exp Brain Res 122:309–317CrossRefPubMed
go back to reference Miscio G, Pisano F, Del Conte C, Pianca D, Colombo R, Schieppati M (2001) The shortening reaction of forearm muscles: the influence of central set. Clin Neurophysiol 112:884–894CrossRefPubMed Miscio G, Pisano F, Del Conte C, Pianca D, Colombo R, Schieppati M (2001) The shortening reaction of forearm muscles: the influence of central set. Clin Neurophysiol 112:884–894CrossRefPubMed
go back to reference Myklebust BM, Gottlieb GL, Penn RD, Agarwal GC (1982) Reciprocal excitation of antagonistic muscles as a differentiating feature of spasticity. Ann Neurol 12:367–374CrossRefPubMed Myklebust BM, Gottlieb GL, Penn RD, Agarwal GC (1982) Reciprocal excitation of antagonistic muscles as a differentiating feature of spasticity. Ann Neurol 12:367–374CrossRefPubMed
go back to reference Nicolas G, Marchand-Pauvert V, Burke D, Pierrot-Deseilligny E (2001) Corticospinal excitation of presumed cervical propriospinal neurones and its reversal to inhibition in humans. J Physiol 533:903–919CrossRefPubMed Nicolas G, Marchand-Pauvert V, Burke D, Pierrot-Deseilligny E (2001) Corticospinal excitation of presumed cervical propriospinal neurones and its reversal to inhibition in humans. J Physiol 533:903–919CrossRefPubMed
go back to reference Nielsen J, Kagamihara Y (1993) The regulation of presynaptic inhibition during co-contraction of antagonist muscles in man. J Physiol 464:575–593PubMed Nielsen J, Kagamihara Y (1993) The regulation of presynaptic inhibition during co-contraction of antagonist muscles in man. J Physiol 464:575–593PubMed
go back to reference Nielsen JB, Pierrot-Deseilligny E (1996) Evidence of facilitation of soleus-coupled Renshaw cells during voluntary co-contraction of antagonistic ankle muscles in man. J Physiol 493:603–611PubMed Nielsen JB, Pierrot-Deseilligny E (1996) Evidence of facilitation of soleus-coupled Renshaw cells during voluntary co-contraction of antagonistic ankle muscles in man. J Physiol 493:603–611PubMed
go back to reference Nielsen J, Petersen N, Deuschl G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471:223–243PubMed Nielsen J, Petersen N, Deuschl G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471:223–243PubMed
go back to reference Nielsen J, Sinkjaer T, Toft E, Kagamihara Y (1994) Segmental reflexes and ankle joint stiffness during co-contraction of antagonistic ankle muscles in man. Exp Brain Res 102:350–358PubMed Nielsen J, Sinkjaer T, Toft E, Kagamihara Y (1994) Segmental reflexes and ankle joint stiffness during co-contraction of antagonistic ankle muscles in man. Exp Brain Res 102:350–358PubMed
go back to reference Osu R, Franklin DW, Kato H, Gomi H, Domen K, Yoshioka T, Kawato M (2002) Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. J Neurophysiol 88:991–1004PubMed Osu R, Franklin DW, Kato H, Gomi H, Domen K, Yoshioka T, Kawato M (2002) Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG. J Neurophysiol 88:991–1004PubMed
go back to reference Perreault EJ, Chen K, Trumbower RD, Lewis GN (2008) Interactions with compliant loads alter stretch reflex gains but not intermuscular coordination. J Neurophysiol 99:2101–2113CrossRefPubMed Perreault EJ, Chen K, Trumbower RD, Lewis GN (2008) Interactions with compliant loads alter stretch reflex gains but not intermuscular coordination. J Neurophysiol 99:2101–2113CrossRefPubMed
go back to reference Pierrot-Deseilligny E (1996) Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneruons. Prog Neurobiol 48:489–517CrossRefPubMed Pierrot-Deseilligny E (1996) Transmission of the cortical command for human voluntary movement through cervical propriospinal premotoneruons. Prog Neurobiol 48:489–517CrossRefPubMed
go back to reference Pierrot-Deseilligny E, Bergego C, Katz R (1982) Reversal in cutaneous control of Ib pathways during human voluntary contraction. Brain Res 233:400–403CrossRefPubMed Pierrot-Deseilligny E, Bergego C, Katz R (1982) Reversal in cutaneous control of Ib pathways during human voluntary contraction. Brain Res 233:400–403CrossRefPubMed
go back to reference Pruszynski JA, Kurtzer I, Scott SH (2008) Rapid motor responses are appropriately tuned to the metrics of a visuospatial task. J Neurophysiol 100:224–238CrossRefPubMed Pruszynski JA, Kurtzer I, Scott SH (2008) Rapid motor responses are appropriately tuned to the metrics of a visuospatial task. J Neurophysiol 100:224–238CrossRefPubMed
go back to reference Rothwell JC, Traub MM, Marsden CD (1980) Influence of voluntary intent on the human long-latency stretch reflex. Nature 286:496–498CrossRefPubMed Rothwell JC, Traub MM, Marsden CD (1980) Influence of voluntary intent on the human long-latency stretch reflex. Nature 286:496–498CrossRefPubMed
go back to reference Selen LPJ, Beek PJ, Van Dieen JH (2006) Impedance is modulated to meet accuracy demands during goal-directed arm movements. Exp Brain Res 172:129–138CrossRefPubMed Selen LPJ, Beek PJ, Van Dieen JH (2006) Impedance is modulated to meet accuracy demands during goal-directed arm movements. Exp Brain Res 172:129–138CrossRefPubMed
go back to reference Shemmell J, Je HA, Perreault EJ (2009) The differential role of motor cortex in stretch reflex modulation induced by changes in environmental mechanics and verbal instruction. J Neurosci 29:13255–13263CrossRefPubMed Shemmell J, Je HA, Perreault EJ (2009) The differential role of motor cortex in stretch reflex modulation induced by changes in environmental mechanics and verbal instruction. J Neurosci 29:13255–13263CrossRefPubMed
go back to reference Smith AM (1981) The coactivation of antagonist muscles. Can J Physiol Pharmacol 59:733–747PubMed Smith AM (1981) The coactivation of antagonist muscles. Can J Physiol Pharmacol 59:733–747PubMed
go back to reference Solomonow M, Baratta R, Bernardi M, Zhou B, Lu Y, Zhu M, Acierno S (1994) Surface and wire EMG crosstalk in neighbouring muscles. J Electromyogr Kinesiol 4:131–142CrossRefPubMed Solomonow M, Baratta R, Bernardi M, Zhou B, Lu Y, Zhu M, Acierno S (1994) Surface and wire EMG crosstalk in neighbouring muscles. J Electromyogr Kinesiol 4:131–142CrossRefPubMed
go back to reference Xia R, Rymer WZ (2005) Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord 43:14–21CrossRefPubMed Xia R, Rymer WZ (2005) Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord 43:14–21CrossRefPubMed
Metadata
Title
Co-contraction modifies the stretch reflex elicited in muscles shortened by a joint perturbation
Authors
Gwyn N. Lewis
Colum D. MacKinnon
Randy Trumbower
Eric J. Perreault
Publication date
01-11-2010
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1-2/2010
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-010-2426-9

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