Skip to main content
SpringerLink
Log in

The formation of extracellular potentials over the innervation zone: Are these potentials affected by changes in fibre membrane properties?

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

Widespread misconceptions still exist regarding the formation of extracellular potentials over the innervation zone: the assumption (1) that the first phase of these potentials mainly reflects the process of initiation of the intracellular action potential (IAP) at the neuromuscular junction and that (2) these potentials are not sensitive to changes in fibre membrane properties (such as changes in the IAP length). Here, we examined the peculiarities of the extracellular potentials detected over the innervation region with the aim to clarify whether the changes in membrane properties are reflected in the amplitude of these potentials. These goals were addressed using a biophysical model of the IAP as well as a convolutional model of EMG generation. Also, the theoretical predictions made by these models were verified experimentally. We showed that only the initial portion of the potentials detected over the innervation zone corresponded to the origination of the IAP at the junction: the remaining (final) portion resulted from the propagation of the IAP along the fibre. It was found that, as radial distance increases, the portion of the rising phase with “propagating character” increased its duration, whereas the duration of the portion with “standing character” remained unchanged. Moreover, a lengthening of the IAP profile resulted in a distinct increase in the amplitude of the first phase of these potentials. These findings were confirmed experimentally and demonstrate that changes in fibre membrane properties influence the amplitude of surface EMG potentials recorded over the innervation zone to the same extent as they do surface potentials recorded elsewhere along the length of the muscle fibres.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Andreassen S, Arendt-Nielsen L (1987) Muscle fibre conduction velocity in motor units of the human anterior tibial muscle: a new size principle parameter. J Physiol 391:561–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Arabadzhiev TI (2013) Peculiarities of extracellular potentials produced by deep muscles. Part 1: single fibre potential fields. Med Biol Eng Comput 51(6):677–686

    Article  CAS  PubMed  Google Scholar 

  3. Arabadzhiev TI, Dimitrov GV, Dimitrova NA (2005) Intracellular action potential generation and extinction strongly affect the sensitivity of M-wave characteristic frequencies to changes in the peripheral parameters with muscle fatigue. J Electromyogr Kinesiol 15(2):159–169

    Article  CAS  PubMed  Google Scholar 

  4. Arabadzhiev TI, Dimitrov VG, Dimitrov GV (2014) The increase in surface EMG could be a misleading measure of neural adaptation during the early gains in strength. Eur J Appl Physiol 114(8):1645–1655

    Article  PubMed  Google Scholar 

  5. Armstrong JB, Rose PK, Vanner S, Bakker GJ, Richmond FJ (1988) Compartmentalization of motor units in the cat neck muscle, biventer cervicis. J Neurophysiol 60:30–45

    CAS  PubMed  Google Scholar 

  6. Bigland-Ritchie B, Kukulka CG, Lippold OC, Woods JJ (1982) The absence of neuromuscular transmission failure in sustained maximal voluntary contractions. J Physiol 330:265–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Botter A, Oprandi G, Lanfranco F, Allasia S, Maffiuletti NA, Minetto MA (2011) Atlas of the muscle motor points for the lower limb: implications for electrical stimulation procedures and electrode positioning. Eur J Appl Physiol 111:2461–2471

    Article  PubMed  Google Scholar 

  8. Buist M, Smith NP, Pullan AJ (2005) Cardiac electromechanics and the forward/inverse problems of electrocardiology. Conf Proc IEEE Eng Med Biol Soc 7:7198–7200

    CAS  PubMed  Google Scholar 

  9. Cupido CM, Galea V, McComas AJ (1996) Potentiation and depression of the M wave in human biceps brachii. J Physiol 491:541–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Dimitrov GV, Dimitrova NA (1998) Precise and fast calculation of the motor unit potentials detected by a point and rectangular plate electrode. Med Eng Phys 20(5):374–381

    Article  CAS  PubMed  Google Scholar 

  11. Dimitrova N (1987) Mathematical modelling of intra- and extracellular potentials generated by active structures: effects of a step change in structure diameter. General Physiol Biophys 6:19–34

    CAS  Google Scholar 

  12. Dimitrova NA, Dimitrov GV (2006) Electromyography (EMG) modeling. In: Metin A (ed) Wiley encyclopedia of biomedical engineering. Wiley, Hoboken

    Google Scholar 

  13. Farina D, Fortunato E, Merletti R (2000) Noninvasive estimation of motor unit conduction velocity distribution using linear electrode arrays. IEEE Trans Biomed Eng 47:380–388

    Article  CAS  PubMed  Google Scholar 

  14. Farina D, Madeleine P, Graven-Nielsen T, Merletti R, Arendt-Nielsen L (2002) Standardising surface electromyogram recordings for assessment of activity and fatigue in the human upper trapezius muscle. Eur J Appl Physiol 86(6):469–478

    Article  PubMed  Google Scholar 

  15. Farina D, Merletti R, Stegeman DF (2004) Biophysics of the generation of EMG signals. In: Merletti R, Parker P (eds) Electromyography: physiology, engineering, and non-invasive applications. IEEE Press, Piscataway, p 89

    Google Scholar 

  16. Goldstein SS, Rall W (1974) Changes of action potential shape and velocity for changing core conductor geometry. Biophys J 14(10):731–757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hanson J (1974) Effects of repetitive stimulation on membrane potentials and twitch in human and rat intercostal muscle fibres. Acta Physiol Scand 92:238–248

    Article  CAS  PubMed  Google Scholar 

  18. Henneman E (1957) Relation between size of neurons and their susceptibility to discharge. Science 126(3287):1345–1347

    Article  CAS  PubMed  Google Scholar 

  19. Hicks A, Fenton J, Garner S, McComas AJ (1989) M wave potentiation during and after muscle activity. J Appl Physiol 66:2606–2610

    CAS  PubMed  Google Scholar 

  20. Keenan KG, Farina D, Merletti R, Enoka RM (2006) Influence of motor unit properties on the size of the simulated evoked surface EMG potential. Exp Brain Res 169(1):37–49

    Article  PubMed  Google Scholar 

  21. Lännergren J, Westerblad H (1987) Action potential fatigue in single skeletal muscle fibers of Xenopus. Acta Physiol Scand 129:311–318

    Article  PubMed  Google Scholar 

  22. Lateva ZC, McGill KC, Burgar CG (1996) Anatomical and electrophysiological determinants of the human thenar compound muscle action potential. Muscle Nerve 19(11):1457–1468

    Article  CAS  PubMed  Google Scholar 

  23. Lüttgau HC (1965) The effect of metabolic inhibitors on the fatigue of the action potential in single muscle fibers. J Physiol (Lond) 178:45–67

    Article  Google Scholar 

  24. McGill KC, Lateva ZC, Xiao S (2001) A model of the muscle action potential for describing the leading edge, terminal wave, and slow afterwave. IEEE Trans Biomed Eng 48(12):1357–1365

    Article  CAS  PubMed  Google Scholar 

  25. McGill KC, Lateva ZC, Marateb HR (2005) EMGLAB: an interactive EMG decomposition program. J Neurosci Methods 149(2):121–133

    Article  PubMed  Google Scholar 

  26. Mesin L, Farina D (2006) An analytical model for surface EMG generation in volume conductors with smooth conductivity variations. IEEE Trans Biomed Eng 53(5):773–779

    Article  PubMed  Google Scholar 

  27. Milner-Brown HS, Stein RB (1975) The relation between the surface electromyogram and muscular force. J Physiol 246:549–569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Mordhorst M, Heidlauf T, Röhrle O (2015) Predicting electromyographic signals under realistic conditions using a multiscale chemo-electro-mechanical finite element model. Interface Focus 5(2):20140076

    Article  PubMed  PubMed Central  Google Scholar 

  29. Nandedkar SD, Barkhaus PE (2007) Contribution of reference electrode to the compound muscle action potential. Muscle Nerve 36(1):87–92

    Article  PubMed  Google Scholar 

  30. Nandedkar S, Stålberg E (1983) Simulation of single muscle fiber action potentials. Med Biol Eng Comput 21:158–165

    Article  CAS  PubMed  Google Scholar 

  31. Neyroud D, Rüttimann J, Mannion AF, Millet GY, Maffiuletti NA, Kayser B, Place N (2013) Comparison of neuromuscular adjustments associated with sustained isometric contractions of four different muscle groups. J Appl Physiol 114(10):1426–1434

    Article  PubMed  Google Scholar 

  32. Plonsey R, Barr RC (1988) Biolectricity: a quantitative approach. Plenum Press, New York, pp 149–155

  33. Rainoldi A, Melchiorri G, Caruso I (2004) A method for positioning electrodes during surface EMG recordings in lower limb muscles. J Neurosci Meth 134(1):37–43

    Article  CAS  Google Scholar 

  34. Rodriguez-Falces J (2013) A novel approach to teach the generation of bioelectrical potentials from a descriptive and quantitative perspective. Adv Physiol Educ 37(4):327–336

    Article  PubMed  Google Scholar 

  35. Rodriguez-Falces J, Navallas Javier, Gila Luis, Latasa Iván, Malanda Armando (2012) Effects of changes in the shape of the intracellular action potential on the peak-to-peak ratio of single muscle fibre potentials. J Electromyogr Kinesiol 22:88–97

    Article  Google Scholar 

  36. Rodriguez-Falces J, Navallas J, Gila L, Malanda A, Dimitrova NA (2012) Influence of the shape of intracellular potentials on the morphology of single-fiber extracellular potentials in human muscle fibers. Med Biol Eng Comput 50(5):447–460

    Article  PubMed  Google Scholar 

  37. Rodriguez-Falces J, Navallas J, Malanda A (2012) A new way to describe intra- and extra-cellular electrical potentials and their generation by excitable cells. Int J Eng Educ 28:674–685

    Google Scholar 

  38. Rodriguez-Falces J, Negro F, Gonzalez-Izal M, Farina D (2013) Spatial distribution of surface action potentials generated by individual motor units in the human biceps brachii muscle. J Electromyogr Kinesiol 23(4):766–777

    Article  PubMed  Google Scholar 

  39. Rodriguez-Falces J, Gila L, Dimitrova NA (2013) The morphology of single muscle fibre potentials - Part I: simulation study of the distortion introduced by the distant-interfering potentials. J Electromyogr Kinesiol 23(1):14–23

    Article  PubMed  Google Scholar 

  40. Stålberg E, Antoni L (1980) Electrophysiological cross section of the motor unit. J Neurol Neurosurg Psychiatry 43(6):469–474

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wilson F, MacLeod A, Barker P (1933) The distribution of the action currents produced by heart muscle and other excitable tissues immersed in extensive conducting media. J Gen Physical 16:423–456

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Electrical and Electronical Engineering, Universidad Pública de Navarra D.I.E.E, Campus de Arrosadía s/n, 31006, Pamplona, Spain

    Javier Rodriguez-Falces

Authors
  1. Javier Rodriguez-Falces
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javier Rodriguez-Falces.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rodriguez-Falces, J. The formation of extracellular potentials over the innervation zone: Are these potentials affected by changes in fibre membrane properties?. Med Biol Eng Comput 54, 1845–1858 (2016). https://doi.org/10.1007/s11517-016-1487-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-016-1487-8

Keywords

Search

Navigation