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Balance control under different passive contributions of the ankle extensors: quiet standing on inclined surfaces

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Human bipedal stance is often modeled as a single inverted pendulum that pivots at the ankle joints in the sagittal plane. Because the center of body mass is usually maintained in front of the ankle joints, ankle extensor torque is continuously required to prevent the body from falling. During quiet standing, both passive and active mechanisms contribute to generate the ankle extensor torque counteracting gravity. This study aimed to investigate the active stabilization mechanism in more detail. Eight healthy subjects were requested to stand quietly on three different surfaces of 1) toes-up, 2) level, and 3) toes-down. Surface electromyogram (EMG) was recorded from the medial head of the gastrocnemius (MG), soleus (SOL), and tibialis anterior muscles. Inclination angle of the body was simultaneously measured. As a result, we found that EMG activities of MG and SOL were lowest during the toes-up standing and highest during the toes-down, indicating that increased (decreased) passive contribution required less (more) extensor torque generated by active muscle contraction. Frequency domain analysis also revealed that sway-related modulation of the ankle extensor activity (0.12–4.03 Hz) was unchanged among the three foot inclinations. On the other hand, isometric contraction strength of these muscles increased as the slope declined (toes-up < level < toes-down). These results support the idea that by regulating the isometric contraction strength, the CNS maintains a constant level of muscle tone and resultant ankle stiffness irrespective of the passive contribution. Such control scheme would be crucial when we consider the low bandwidth of the intermittent controller.

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  • Bottaro A, Casadio M, Morasso PG, Sanguineti V (2005) Body sway during quiet standing: is it the residual chattering of an intermittent stabilization process? Hum Mov Sci 24:588–615

    Article  PubMed  Google Scholar 

  • Casadio M, Morasso PG, Sanguineti V (2005) Direct measurement of ankle stiffness during quiet standing: implications for control modeling and clinical application. Gait Posture 21:410–423

    Article  PubMed  Google Scholar 

  • Collins JJ, DeLuca CJ (1993) Open-loop and close-loop control of posture: a random-walk analysis of enter-of-pressure trajectories. Exp Brain Res 95:308–318

    Article  PubMed  CAS  Google Scholar 

  • Fitzpatrick RC, Taylor JL, McCloskey DI (1992) Ankle stiffness of standing humans in response to imperceptive perturbation: reflex and task-dependent components. J Physiol 454:533–547

    PubMed  CAS  Google Scholar 

  • Gage WH, Winter DA, Frank JS, Adkin AL (2004) Kinematic and kinetic validity of the inverted pendulum model in quiet standing. Gait Posture 19:124–132

    Article  PubMed  Google Scholar 

  • Gatev P, Thomas S, Kepple T, Hallett M (1999) Feedforward ankle strategy of balance during quiet stance in adults. J Physiol 514:915–928

    Article  PubMed  CAS  Google Scholar 

  • Jeka JJ, Oie KS, Schöner GS, Dijkstra TMH, Henson E (1998) Position and velocity coupling of postural sway to somatosensory drive. J Neurophysiol 79:1661–1674

    PubMed  CAS  Google Scholar 

  • Johnson MA, Polgar J, Weightman D, Applenton D (1973) Data on the distribution of fiber types in thirty-six human muscles an autopsy study. J Neurol Sci 18:111–129

    Article  PubMed  CAS  Google Scholar 

  • Kawakami Y, Ichinose Y, Fukunaga T (1998) Architectural and functional features of human triceps surae muscles during contraction. J Appl Physiol 85:398–404

    PubMed  CAS  Google Scholar 

  • Kawakami Y, Kumagai K, Huijing PA, Hijikata T, Fukunaga T (2000) The length–force characteristics of human gastrocnemius and soleus muscles in vivo. In: Herzog W (ed) Skeletal muscle mechanics: from mechanisms to function. Wiley, London, pp 321–341

    Google Scholar 

  • Kouzaki M, Fukunaga T (2008) Frequency features of mechanomyographic signals of human soleus muscle during quiet standing. J Neurosci Methods 173:241–248

    Article  PubMed  Google Scholar 

  • Lakie M, Caplan N, Loram ID (2003) Human balancing of an inverted pendulum with a compliant linkage: neural control by anticipatory intermittent bias. J Physiol 551:357–370

    Article  PubMed  CAS  Google Scholar 

  • Loram ID, Lakie M (2002) Direct measurement of human ankle stiffness during quiet standing: the intrinsic mechanical stiffness is insufficient for stability. J Physiol 545:1041–1053

    Article  PubMed  CAS  Google Scholar 

  • Loram ID, Maganaris CN, Lakie M (2005) Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius. J Physiol 564:295–311

    Article  PubMed  CAS  Google Scholar 

  • Loram ID, Gawthrop PJ, Lakie M (2006) The frequency of human, manual adjustments in balancing an inverted pendulum is constrained by intrinsic physiological factors. J Physiol 577:417–432

    Article  PubMed  CAS  Google Scholar 

  • Loram ID, Maganaris CN, Lakie M (2007) The passive, human calf muscles in relation to standing: the non-linear decrease from short range to long range stiffness. J Physiol 584:661–675

    Article  PubMed  CAS  Google Scholar 

  • Löscher WN, Gallasch E (1993) Myo-electric signals from two extrinsic hand muscles and force tremor during isometric handgrip. Eur J Appl Physiol 67:99–105

    Article  Google Scholar 

  • Masani K, Nakazawa K, Kouzaki M (2001) Two frequency components in ankle extensor activity during human quiet standing. Soc Neurosci Abstr 305:2

    Google Scholar 

  • 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 90:3774–3782

    Article  PubMed  Google Scholar 

  • Masani K, Vette AH, Popovic MR (2006) Controlling balance during quiet standing: proportional and derivative controller generates preceding motor command to body sway position observed in experiments. Gait Posture 23:164–172

    Article  PubMed  Google Scholar 

  • Masani K, Vette AH, Kouzaki M, Kanehisa H, Fukunaga T, Popovic MR (2007) Larger center of pressure minus center of gravity in the elderly induces larger body acceleration during quiet standing. Neurosci Lett 422:202–206

    Article  PubMed  CAS  Google Scholar 

  • McAuley JH, Marsden CD (2000) Physiological and pathological tremor and rhythmic central motor control. Brain 123:1545–1567

    Article  PubMed  Google Scholar 

  • Mezzarane RA, Kohn AF (2007) Control of upright stance over inclined surfaces. Exp Brain Res 180:377–388

    Article  PubMed  Google Scholar 

  • Morasso PG, Sanguineti V (2002) Ankle muscle stiffness alone cannot stabilize balance during quiet standing. J Neurophysiol 88:2157–2162

    PubMed  Google Scholar 

  • Mori S (1973) Discharge patterns of soleus motor units with associated changes in force exerted by foot during quiet standing in man. J Neurophysiol 36:458–471

    PubMed  CAS  Google Scholar 

  • Mori S (1975) Entrainment of motor-unit discharges as a neuronal mechanism of synchronization. J Neurophysiol 38:859–870

    PubMed  CAS  Google Scholar 

  • Nozaki D, Hirano T, Nakazawa K, Akai M (2004) Cosine tuning can predict different activity patterns among triceps surae muscles during human quiet standing. Soc Neurosci Abstr 306:5

    Google Scholar 

  • Peterka RJ (2002) Sensorimotor integration in human postural control. J Neurophysiol 88:1097–1118

    PubMed  CAS  Google Scholar 

  • Smith JW (1957) The forces operating at the human ankle joint during standing. J Anat 91:545–564

    PubMed  CAS  Google Scholar 

  • Winter DA, Patla AE, Prince F, Ishac M, Gielo-Perczak K (1998) Stiffness control of balance in quiet standing. J Neurophysiol 80:1211–1221

    PubMed  CAS  Google Scholar 

  • Winter DA, Patla AE, Rietdyk S, Ishac MG (2001) Ankle muscle stiffness in the control of balance during quiet standing. J Neurophysiol 85:2630–2633

    PubMed  CAS  Google Scholar 

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We thank K. Yaeshima for his helpful advice. We also thank Y. Inaba for her assistance in manuscript preparation.

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Correspondence to Shun Sasagawa.

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Sasagawa, S., Ushiyama, J., Masani, K. et al. Balance control under different passive contributions of the ankle extensors: quiet standing on inclined surfaces. Exp Brain Res 196, 537–544 (2009).

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