Skip to main content

Advertisement

Log in

Foot equilibrium position controls partition of voluntary command to antagonists during foot oscillations

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

Abstract

During low-frequency (<1.5 Hz) voluntary oscillations of the foot, placed on a rotating platform, onset of the Tibialis Anterior (TA) EMG paradoxically phase-lags the onset of dorsiflexion, suggesting that initial dorsiflexion is sustained by recoil of elastic structures that were stretched during plantarflexion. It is argued that the lag would disappear if the EMG onset were referred to the foot passive equilibrium position rather than to the movement onset. This hypothesis was tested in ten subjects who, after assessment of foot equilibrium position, voluntarily oscillated their foot at various frequencies (0.2–3 Hz) over three angular ranges: a mid range (foot crossing the equilibrium symmetrically), a high range (whole excursion above equilibrium) and a low range (whole excursion below equilibrium). In the mid range, phase relations were measured between the crossing of equilibrium position and the onset of the TA EMG during dorsiflexion or the onset of Soleus EMG during plantarflexion. In both cases, the paradoxical lag of EMG on movement was absent, phase curves started around zero and could be well fitted by a second order model. Phase curves with similar features were also obtained in the high and low ranges (no crossing of equilibrium) but correlating the onset of the EMG burst to the onset of the related movement. Altogether, these findings show that in all ranges of the joint excursion, the homology is between the EMG onset and the moment when the foot draws away from equilibrium. Based on the observed pattern of muscular activation, we suggest that voluntary foot oscillation in any movement range is sustained by one sinusoidal central command that, when equilibrium is crossed, is clipped in two half-waves reciprocally distributed to the couple of antagonist muscles. A simple neural circuit for this operation is proposed.

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. 1A–C
Fig. 2A–D
Fig. 3A–D
Fig. 4

Similar content being viewed by others

References

  • Baldissera F, Cavallari P (2001) Neural compensation for mechanical loading of the hand during coupled oscillations of the hand and foot. Exp Brain Res 139:18–29

    CAS  PubMed  Google Scholar 

  • Baldissera F, Cavallari P, Civaschi P (1982) Preferential coupling between voluntary movements of ipsilateral limbs. Neurosci Lett 34:95–100

    CAS  PubMed  Google Scholar 

  • Baldissera F, Cavallari P, Marini G, Tassone G (1991) Differential control of in-phase and anti-phase coupling of rhythmic movements of ipsilateral hand and foot. Exp Brain Res 83:375–380

    CAS  PubMed  Google Scholar 

  • Baldissera F, Borroni P, Cavallari P (2000) Neural compensation for mechanical differences between hand and foot during coupled oscillations of the two segments. Exp Brain Res 133:165–177

    CAS  PubMed  Google Scholar 

  • Bobet J, Stein RB, Oguztöreli MN (1990) Mechanisms relating force and high-frequency stiffness in skeletal muscle. J Biomech 23[Suppl 1]: 13–21

  • Butler EG, Horne MK, Hawkins NJ (1992) The activity of monkey thalamic and motor cortical neurones in a skilled, ballistic movement. J Physiol 445:25–48

    CAS  PubMed  Google Scholar 

  • Butler EG, Finkelstein DI, Harvey MC, Churchward PR, Forlano LM, Horne MK (1996) The relationship between monkey ventrolateral thalamic nucleus activity and kinematic parameters of wrist movement. Brain Res 736:146–159

    CAS  PubMed  Google Scholar 

  • Carson RG (1993) Manual asymmetries: old problems and new directions. Hum Mov Sci 12:479–506

    Article  Google Scholar 

  • Carson RG, Goodman D, Kelso JAS, Elliott D (1995) Phase transitions and critical fluctuations in rhythmic coordination of ipsilateral hand and foot. J Mot Behav 27:211–224

    PubMed  Google Scholar 

  • Carson RG, Riek S, Smethurst CJ, Parraga JF, Byblow WD (2000) Neuromuscular-skeletal constraints upon the dynamics of unimanual and bimanual coordination. Exp Brain Res 131:196–214

    CAS  PubMed  Google Scholar 

  • Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44:773–791

    CAS  PubMed  Google Scholar 

  • Cheney PD, Kasser R, Holsapple J (1982) Reciprocal effect of single corticomotoneuronal cells on wrist extensor and flexor muscle activity in the primate. Brain Res 247:164–168

    Article  CAS  PubMed  Google Scholar 

  • Christopoulos A (1998) Assessing the distribution of parameters in models of ligand-receptors interaction: to log or not to log. Trends Pharmacol Sci 19:351–357

    CAS  PubMed  Google Scholar 

  • Fetz EE, Perlmutter SI, Prut Y, Seki K, Votaw S (2002) Roles of primate spinal interneurones in preparation and execution of voluntary hand movement. Brain Res Rev 40:53–65

    Article  CAS  PubMed  Google Scholar 

  • Hunter IW, Kearney RE (1982) Dynamics of human ankle stiffness: variation with men ankle torque. J Biomech 15:747–752

    CAS  PubMed  Google Scholar 

  • Jeka JJ, Kelso JAS (1995) Manipulating symmetry in the coordination dynamics of human movement. J Exp Psychol Hum Percept Perform 21:360–374

    CAS  PubMed  Google Scholar 

  • Kelso JAS (1984) Phase transitions and critical behaviour in human bimanual coordination. Am J Physiol 246:R1000–R1004

    CAS  PubMed  Google Scholar 

  • Kelso JAS, Jeka JJ (1992) Symmetry breaking dynamics of human inter-limb coordination. J Exp Psychol Hum Percept Perform 18:645–668

    CAS  PubMed  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 

  • Lehman SL, Calhoun BM (1990) An identified model for human wrist movements. Exp Brain Res 81:199–208

    CAS  PubMed  Google Scholar 

  • Levin MF, Dimov M (1997) Spatial zones for muscle coactivation and the control of postural stability. Brain Res 757:43–59

    CAS  PubMed  Google Scholar 

  • Maier MA, Perlmutter SI, Fetz EE (1998) Response patterns and force relations of monkey spinal interneurons during active wrist movement. J Neurophysiol 80:2495–2513

    CAS  PubMed  Google Scholar 

  • Mewes K, Cheney PD (1994) Primate rubromotoneuronal cells: parametric relations and contribution to wrist movement. J Neurophysiol 72:14–30

    CAS  PubMed  Google Scholar 

  • Motulsky H (1999) Analyzing data with the GraphPad Prism. GraphPad Software, San Diego

  • Perlmutter SI, Maier MA, Fetz EE (1998) Activity of spinal interneurons and their effects on forearm muscles during voluntary wrist movements in the monkey. J Neurophysiol 80:2475–2494

    CAS  PubMed  Google Scholar 

  • Serrien DJ, Swinnen SP (1998) Load compensation during homologous and non-homologous coordination. Exp Brain Res 121:223–229

    Article  CAS  PubMed  Google Scholar 

  • Stark LS (1968) Neurological control systems. Studies in Bioengineering. Plenum Press, New York

  • Stiles RN (1983) Lightly damped hand oscillations: acceleration-related feedback and system damping. J Neurophysiol 50:327–343

    CAS  PubMed  Google Scholar 

  • Swinnen SP, Dounskaia N, Verschueren S, Serrien DJ, Daelman A (1995) Relative phase destabilization during inter-limb coordination: the disruptive role of kinesthetic afferences induced by passive movement. Exp Brain Res 105:439–454

    CAS  PubMed  Google Scholar 

  • Viviani P, Soechting JF, Terzuolo CA (1976) Influence of mechanical properties of the relation between EMG activity and torque. J Physiol (Paris) 72:45–58

    Google Scholar 

  • Weiss PL, Kearney RE, Hunter IW (1986a) Position dependence of ankle joint dynamics—I. Passive mechanics. J Biomech 19:727–735

    CAS  PubMed  Google Scholar 

  • Weiss PL, Kearney RE, Hunter IW (1986b) Position dependence of ankle joint dynamics—II. Active mechanics. J Biomech 19:737–751

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by the “Ministero della Università e della Ricerca” and the “Università degli Studi di Milano”. We are indebted to Eberhard Fetz for helpful comments and suggestions on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fausto Baldissera.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baldissera, F., Cavallari, P. & Esposti, R. Foot equilibrium position controls partition of voluntary command to antagonists during foot oscillations. Exp Brain Res 155, 274–282 (2004). https://doi.org/10.1007/s00221-003-1723-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-003-1723-y

Keywords

Navigation