Skip to main content
Top
Published in: Experimental Brain Research 4/2006

01-11-2006 | Research Article

Low-frequency common modulation of soleus motor unit discharge is enhanced during postural control in humans

Authors: G. Mochizuki, J. G. Semmler, T. D. Ivanova, S. J. Garland

Published in: Experimental Brain Research | Issue 4/2006

Login to get access

Abstract

The maintenance of quiet stance requires the activation of muscles bilaterally. The soleus muscles in each leg share a common function in standing; that is, each muscle acts to control antero-posterior (AP) sway on its own side. We sought to determine the extent to which oscillations in motor unit discharge were related in motor unit pairs of the soleus muscles during postural and voluntary isometric tasks, both within and between legs. Subjects stood quietly for 5 min or performed a voluntary isometric plantarflexion contraction in a seated position. During the postural tasks, the excursions of AP sway between legs were highly correlated (ρ = 0.86 ± 0.06). The strength of common modulation of motor unit discharge rates was assessed using time- and frequency-domain analyses. The time-domain common drive analysis revealed that the strongest correlation in motor unit discharge modulation occurred in the postural task with unilateral pairs (ρ = 0.71 ± 0.13) being more strongly correlated than bilateral pairs (ρ = 0.50 ± 0.16). Common modulation of motor unit discharge was lowest for the voluntary tasks, with ρ = 0.38 ± 0.11 and 0.16 ± 0.08 for unilateral and bilateral pairs, respectively. Similarly, the frequency-domain coherence analysis demonstrated an identical ordering effect, with the largest maximum pooled coherence occurring during standing posture in unilateral (0.070 at 1.6 Hz) and bilateral (0.055 at 1.6 Hz) recordings, whereas minimal coherence was observed in the voluntary task in both unilateral and bilateral recordings within the 0–5 Hz range. These results indicate that in the soleus muscle, common modulation of motor unit discharge is greater during postural tasks than during voluntary isometric tasks and can be observed in both bilateral and unilateral motor unit pairs. Differences in the extent of co-modulation of motor unit discharge between tasks may be attributed to either differences in the descending control or differences in the proprioceptive input between postural and isometric tasks.
Literature
go back to reference Adam A, De Luca CJ (2005) Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. J Appl Physiol 99:268–280PubMedCrossRef Adam A, De Luca CJ (2005) Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. J Appl Physiol 99:268–280PubMedCrossRef
go back to reference Amjad AM, Halliday DM, Rosenberg JR, Conway BA (1997) An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor. J Neurosci Methods 73:69–79PubMedCrossRef Amjad AM, Halliday DM, Rosenberg JR, Conway BA (1997) An extended difference of coherence test for comparing and combining several independent coherence estimates: theory and application to the study of motor units and physiological tremor. J Neurosci Methods 73:69–79PubMedCrossRef
go back to reference Andreassen S, Rosenfalck A (1980) Regulation of the firing pattern of single motor units. J Neurol Neurosurg Psychiatry 43:897–906PubMed Andreassen S, Rosenfalck A (1980) Regulation of the firing pattern of single motor units. J Neurol Neurosurg Psychiatry 43:897–906PubMed
go back to reference Bellemare F, Woods JJ, Johansson R, Bigland-Ritchie B (1983) Motor-unit discharge rates in maximal voluntary contractions of three human muscles. J Neurophysiol 50:1380–1392PubMed Bellemare F, Woods JJ, Johansson R, Bigland-Ritchie B (1983) Motor-unit discharge rates in maximal voluntary contractions of three human muscles. J Neurophysiol 50:1380–1392PubMed
go back to reference Brouwer B, Ashby P (1990) Corticospinal projections to upper and lower limb spinal motoneurons in man. Electroencephalogr Clin Neurophysiol 76:509–519PubMedCrossRef Brouwer B, Ashby P (1990) Corticospinal projections to upper and lower limb spinal motoneurons in man. Electroencephalogr Clin Neurophysiol 76:509–519PubMedCrossRef
go back to reference Brouwer B, Ashby P (1992) Corticospinal projections to lower limb motoneurons in man. Exp Brain Res 89:649–654PubMedCrossRef Brouwer B, Ashby P (1992) Corticospinal projections to lower limb motoneurons in man. Exp Brain Res 89:649–654PubMedCrossRef
go back to reference Davey NJ, Ellaway PH, Baker JR, Friedland CL (1993) Rhythmicity associated with a high degree of short-term synchrony of motor unit discharge in man. Exp Physiol 78:649–661PubMed Davey NJ, Ellaway PH, Baker JR, Friedland CL (1993) Rhythmicity associated with a high degree of short-term synchrony of motor unit discharge in man. Exp Physiol 78:649–661PubMed
go back to reference De Luca CJ, Erim Z (2002) Common drive in motor units of a synergistic muscle pair. J Neurophysiol 87:2200–2204PubMed De Luca CJ, Erim Z (2002) Common drive in motor units of a synergistic muscle pair. J Neurophysiol 87:2200–2204PubMed
go back to reference De Luca CJ, LeFever RS, McCue MP, Xenakis AP (1982) Control scheme governing concurrently active human motor units during voluntary contractions. J Physiol 329:129–142PubMed De Luca CJ, LeFever RS, McCue MP, Xenakis AP (1982) Control scheme governing concurrently active human motor units during voluntary contractions. J Physiol 329:129–142PubMed
go back to reference Dietz V, Horstmann GA, Berger W (1989) Interlimb coordination of leg-muscle activation during perturbation of stance in humans. J Neurophysiol 62:680–693PubMed Dietz V, Horstmann GA, Berger W (1989) Interlimb coordination of leg-muscle activation during perturbation of stance in humans. J Neurophysiol 62:680–693PubMed
go back to reference Erim Z, Beg MF, Burke DT, De Luca CJ (1999) Effects of aging on motor-unit control properties. J Neurophysiol 82:2081–2091PubMed Erim Z, Beg MF, Burke DT, De Luca CJ (1999) Effects of aging on motor-unit control properties. J Neurophysiol 82:2081–2091PubMed
go back to reference Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, Stephens JA (1993) The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470:127–155PubMed Farmer SF, Bremner FD, Halliday DM, Rosenberg JR, Stephens JA (1993) The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470:127–155PubMed
go back to reference Fitzpatrick RC, Gorman RB, Burke D, Gandevia SC (1992) Postural proprioceptive reflexes in standing human subjects: bandwidth of response and transmission characteristics. J Physiol 458:69–83PubMed Fitzpatrick RC, Gorman RB, Burke D, Gandevia SC (1992) Postural proprioceptive reflexes in standing human subjects: bandwidth of response and transmission characteristics. J Physiol 458:69–83PubMed
go back to reference Garland SJ, Miles TS (1997) Control of motor units in human flexor digitorum profundus under different proprioceptive conditions. J Physiol 502:693–701PubMedCrossRef Garland SJ, Miles TS (1997) Control of motor units in human flexor digitorum profundus under different proprioceptive conditions. J Physiol 502:693–701PubMedCrossRef
go back to reference Gatev P, Thomas S, Kepple T, Hallett M (1999) Feedforward ankle strategy of balance during quiet stance in adults. J Physiol 514:915–928PubMedCrossRef Gatev P, Thomas S, Kepple T, Hallett M (1999) Feedforward ankle strategy of balance during quiet stance in adults. J Physiol 514:915–928PubMedCrossRef
go back to reference Halliday DM, Conway BA, Christensen LO, Hansen NL, Petersen NP, Nielsen JB (2003) Functional coupling of motor units is modulated during walking in human subjects. J Neurophysiol 89:960–968PubMedCrossRef Halliday DM, Conway BA, Christensen LO, Hansen NL, Petersen NP, Nielsen JB (2003) Functional coupling of motor units is modulated during walking in human subjects. J Neurophysiol 89:960–968PubMedCrossRef
go back to reference Hayashi R, Miyake A, Jijiwa H, Watanabe S (1981) Postural readjustment to body sway induced by vibration in man. Exp Brain Res 43:217–225PubMedCrossRef Hayashi R, Miyake A, Jijiwa H, Watanabe S (1981) Postural readjustment to body sway induced by vibration in man. Exp Brain Res 43:217–225PubMedCrossRef
go back to reference Horak FB, Earhart GM, Dietz V (2001) Postural responses to combinations of head and body displacements: vestibular-somatosensory interactions. Exp Brain Res 141:410–414PubMedCrossRef Horak FB, Earhart GM, Dietz V (2001) Postural responses to combinations of head and body displacements: vestibular-somatosensory interactions. Exp Brain Res 141:410–414PubMedCrossRef
go back to reference Iyer MB, Christakos CN, Ghez C (1994) Coherent modulations of human motor unit discharges during quasi-sinusoidal isometric muscle contractions. Neurosci Lett 170:94–98PubMedCrossRef Iyer MB, Christakos CN, Ghez C (1994) Coherent modulations of human motor unit discharges during quasi-sinusoidal isometric muscle contractions. Neurosci Lett 170:94–98PubMedCrossRef
go back to reference Kavounoudias A, Roll R, Roll JP (2001) Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation. J Physiol 532:869–878PubMedCrossRef Kavounoudias A, Roll R, Roll JP (2001) Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation. J Physiol 532:869–878PubMedCrossRef
go back to reference Keen DA, Fuglevand AJ (2004) Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. J Neurophysiol 91:57–62PubMedCrossRef Keen DA, Fuglevand AJ (2004) Common input to motor neurons innervating the same and different compartments of the human extensor digitorum muscle. J Neurophysiol 91:57–62PubMedCrossRef
go back to reference Kim MS, Masakado Y, Tomita Y, Chino N, Pae YS, Lee KE (2001) Synchronization of single motor units during voluntary contractions in the upper and lower extremities. Clin Neurophysiol 112:1243–1249PubMedCrossRef Kim MS, Masakado Y, Tomita Y, Chino N, Pae YS, Lee KE (2001) Synchronization of single motor units during voluntary contractions in the upper and lower extremities. Clin Neurophysiol 112:1243–1249PubMedCrossRef
go back to reference Kuchinad RA, Ivanova TD, Garland SJ (2004) Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle. Exp Brain Res 158:345–355PubMedCrossRef Kuchinad RA, Ivanova TD, Garland SJ (2004) Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle. Exp Brain Res 158:345–355PubMedCrossRef
go back to reference Loram ID, Maganaris CN, Lakie M (2005) Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius. J Physiol 564:295–311PubMedCrossRef Loram ID, Maganaris CN, Lakie M (2005) Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius. J Physiol 564:295–311PubMedCrossRef
go back to reference Marsden JF, Farmer SF, Halliday DM, Rosenberg JR, Brown P (1999) The unilateral and bilateral control of motor unit pairs in the first dorsal interosseous and paraspinal muscles in man. J Physiol 521:553–564PubMedCrossRef Marsden JF, Farmer SF, Halliday DM, Rosenberg JR, Brown P (1999) The unilateral and bilateral control of motor unit pairs in the first dorsal interosseous and paraspinal muscles in man. J Physiol 521:553–564PubMedCrossRef
go back to reference Masani K, Popovic MR, Nakazawa K, Kouzaki M, Nozaki D (2003) Importance of body sway velocity information in controlling ankle extensor activities during quiet stance. J Neurophysiol 90:3774–3782PubMedCrossRef Masani K, Popovic MR, Nakazawa K, Kouzaki M, Nozaki D (2003) Importance of body sway velocity information in controlling ankle extensor activities during quiet stance. J Neurophysiol 90:3774–3782PubMedCrossRef
go back to reference Mauritz KH, Dietz V (1980) Characteristics of postural instability induced by ischemic blocking of leg afferents. Exp Brain Res 38:117–119PubMedCrossRef Mauritz KH, Dietz V (1980) Characteristics of postural instability induced by ischemic blocking of leg afferents. Exp Brain Res 38:117–119PubMedCrossRef
go back to reference Mochizuki G, Ivanova TD, Garland SJ (2004) Postural muscle activity during bilateral and unilateral arm movements at different speeds. Exp Brain Res 155:352–361PubMedCrossRef Mochizuki G, Ivanova TD, Garland SJ (2004) Postural muscle activity during bilateral and unilateral arm movements at different speeds. Exp Brain Res 155:352–361PubMedCrossRef
go back to reference Mochizuki G, Ivanova TD, Garland SJ (2005) Synchronization of motor units in human soleus muscle during standing postural tasks. J Neurophysiol 94:62–69PubMedCrossRef Mochizuki G, Ivanova TD, Garland SJ (2005) Synchronization of motor units in human soleus muscle during standing postural tasks. J Neurophysiol 94:62–69PubMedCrossRef
go back to reference Moritz CT, Christou EA, Meyer FG, Enoka RM (2005) Coherence at 16-32 Hz can be caused by short-term synchrony of motor units. J Neurophysiol 94:105–118PubMedCrossRef Moritz CT, Christou EA, Meyer FG, Enoka RM (2005) Coherence at 16-32 Hz can be caused by short-term synchrony of motor units. J Neurophysiol 94:105–118PubMedCrossRef
go back to reference Oda S, Moritani T (1995) Cross-correlation of bilateral differences in fatigue during sustained maximal voluntary contraction. Eur J Appl Physiol Occup Physiol 70:305–310PubMedCrossRef Oda S, Moritani T (1995) Cross-correlation of bilateral differences in fatigue during sustained maximal voluntary contraction. Eur J Appl Physiol Occup Physiol 70:305–310PubMedCrossRef
go back to reference Person RS, Kudina LP (1972) Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. Electroencephalogr Clin Neurophysiol 32:471–483PubMedCrossRef Person RS, Kudina LP (1972) Discharge frequency and discharge pattern of human motor units during voluntary contraction of muscle. Electroencephalogr Clin Neurophysiol 32:471–483PubMedCrossRef
go back to reference Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118PubMed Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118PubMed
go back to reference Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53:1–31PubMedCrossRef Rosenberg JR, Amjad AM, Breeze P, Brillinger DR, Halliday DM (1989) The Fourier approach to the identification of functional coupling between neuronal spike trains. Prog Biophys Mol Biol 53:1–31PubMedCrossRef
go back to reference Sears TA, Stagg D (1976) Short-term synchronization of intercostal motoneurone activity. J Physiol 263:357–381PubMed Sears TA, Stagg D (1976) Short-term synchronization of intercostal motoneurone activity. J Physiol 263:357–381PubMed
go back to reference Semmler JG, Kornatz KW, Dinenno DV, Zhou S, Enoka RM (2002) Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J Physiol 545:681–695PubMedCrossRef Semmler JG, Kornatz KW, Dinenno DV, Zhou S, Enoka RM (2002) Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J Physiol 545:681–695PubMedCrossRef
go back to reference Semmler JG, Nordstrom MA (1998) Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp Brain Res 119:27–38PubMedCrossRef Semmler JG, Nordstrom MA (1998) Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp Brain Res 119:27–38PubMedCrossRef
go back to reference Semmler JG, Nordstrom MA, Wallace CJ (1997) Relationship between motor unit short-term synchronization and common drive in human first dorsal interosseous muscle. Brain Res 767:314–320PubMedCrossRef Semmler JG, Nordstrom MA, Wallace CJ (1997) Relationship between motor unit short-term synchronization and common drive in human first dorsal interosseous muscle. Brain Res 767:314–320PubMedCrossRef
go back to reference Semmler JG, Sale MV, Meyer FG, Nordstrom MA (2004) Motor-unit coherence and its relation with synchrony are influenced by training. J Neurophysiol 92:3320–3331PubMedCrossRef Semmler JG, Sale MV, Meyer FG, Nordstrom MA (2004) Motor-unit coherence and its relation with synchrony are influenced by training. J Neurophysiol 92:3320–3331PubMedCrossRef
go back to reference Sturm H, Schmied A, Vedel JP, Pagni S (1997) Firing pattern of type-identified wrist extensor motor units during wrist extension and hand clenching in humans. J Physiol 504:735–745PubMedCrossRef Sturm H, Schmied A, Vedel JP, Pagni S (1997) Firing pattern of type-identified wrist extensor motor units during wrist extension and hand clenching in humans. J Physiol 504:735–745PubMedCrossRef
go back to reference Westgaard RH, De Luca CJ (2001) Motor control of low-threshold motor units in the human trapezius muscle. J Neurophysiol 85:1777–1781PubMed Westgaard RH, De Luca CJ (2001) Motor control of low-threshold motor units in the human trapezius muscle. J Neurophysiol 85:1777–1781PubMed
go back to reference Winter DA, Patla AE, Prince F, Ishac MG, Gielo-Perczak K (1998) Stiffness control of balance in quiet standing. J Neurophysiol 80:1211–1221PubMed Winter DA, Patla AE, Prince F, Ishac MG, Gielo-Perczak K (1998) Stiffness control of balance in quiet standing. J Neurophysiol 80:1211–1221PubMed
go back to reference Winter DA, Patla AE, Rietdyk S, Ishac MG (2001) Ankle muscle stiffness in the control of balance during quiet standing. J Neurophysiol 85:2630–2633PubMed Winter DA, Patla AE, Rietdyk S, Ishac MG (2001) Ankle muscle stiffness in the control of balance during quiet standing. J Neurophysiol 85:2630–2633PubMed
go back to reference Winter DA, Prince F, Stergiou P, Powell C (1993) Medial–lateral and anterior–posterior motor responses associated with centere of pressure changes in quiet standing. Neurosci Res Commun 12:141–148 Winter DA, Prince F, Stergiou P, Powell C (1993) Medial–lateral and anterior–posterior motor responses associated with centere of pressure changes in quiet standing. Neurosci Res Commun 12:141–148
go back to reference Zattara M, Bouisset S (1988) Posturo-kinetic organisation during the early phase of voluntary upper limb movement. 1. Normal subjects. J Neurol Neurosurg Psychiatry 51:956–965CrossRef Zattara M, Bouisset S (1988) Posturo-kinetic organisation during the early phase of voluntary upper limb movement. 1. Normal subjects. J Neurol Neurosurg Psychiatry 51:956–965CrossRef
Metadata
Title
Low-frequency common modulation of soleus motor unit discharge is enhanced during postural control in humans
Authors
G. Mochizuki
J. G. Semmler
T. D. Ivanova
S. J. Garland
Publication date
01-11-2006
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 4/2006
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-006-0575-7

Other articles of this Issue 4/2006

Experimental Brain Research 4/2006 Go to the issue