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Neurological Sciences

, Volume 37, Issue 1, pp 37–43 | Cite as

Motor unit firing pattern: evidence for motoneuronal or axonal discharge origin?

  • Lydia P. Kudina
  • Regina E. Andreeva
Original Article

Abstract

In neuromuscular diseases, a fasciculation origin is disputed. In some reports, it was suggested that motor unit firing pattern alone is evidence for motoneuronal or axonal fasciculations; namely interspike intervals of approximately 5 ms (doublet intervals) provide evidence for the axonal firing. To clarify the reliability of the suggestion, we compared doublet intervals originated in motoneurons and their axons in healthy humans. For this aim, the H-reflex and M-response of single motor units were elicited during gentle voluntary muscle contractions. Peri-stimulus time histograms allowed reliable judgment about a doublet origin: motoneuronal (at the H-reflex latency) or axonal (at the M-response latency). Significant difference between motoneuronal and axonal doublet intervals was absent. It was concluded that doublet interval alone cannot be the reliable criterion for an axonal firing origin; additional evidences are needed for this conclusion, for example, the appearance of the F-wave. The approach may be used as an additional estimation of mechanisms underlying motor unit diseases.

Keywords

Human firing motor units Axonal and motoneuronal double discharges Fasciculation potentials Interspike interval analysis 

Notes

Acknowledgments

The authors thank Dr. M. Piotrkiewicz (Nałęcz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw) who has kindly provided the analysis software.

Compliance with ethical standards

Conflict of interest

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

References

  1. 1.
    de Carvalho M, Swash M (2012) Fasciculation potentials: still mysterious. Clin Neurophysiol 123:227–228. doi: 10.1016/j.clinph.2011.07.002 PubMedCrossRefGoogle Scholar
  2. 2.
    Roth G (1984) Fasciculations and their F-response: localization of their axonal origin. J Neurol Sci 63:299–306PubMedCrossRefGoogle Scholar
  3. 3.
    Kuwabara S, Shibuya K, Misawa S (2014) Fasciculations, axonal hyperexcitability, and motoneuronal death in amyotrophic lateral sclerosis. Clin Neurophysiol 125:872–873. doi: 10.1016/j.clinph.2013.11.014 PubMedCrossRefGoogle Scholar
  4. 4.
    Guiloff RJ, Modarres-Sadeghi H (1992) Voluntary activation and fiber density of fasciculations in motor neuron disease. Ann Neurol 31:416–424. doi: 10.1002/ana.410310411 PubMedCrossRefGoogle Scholar
  5. 5.
    de Carvalho M, Miranda PC, Lourdes Sales Luís M, Ducla-Soares E (2000) Neurophysiological features of fasciculation potentials evoked by transcranial magnetic stimulation in amyotrophic lateral sclerosis. J Neurol 247:189–194. doi: 10.1007/s004150050561 PubMedCrossRefGoogle Scholar
  6. 6.
    Mills KR (2010) Characteristics of fasciculations in amyotrophic lateral sclerosis and the benign fasciculation syndrome. Brain 133:3458–3469. doi: 10.1093/brain/awq290 PubMedCrossRefGoogle Scholar
  7. 7.
    de Carvalho M, Swash M (1998) Fasciculation potentials: a study of amyotrophic lateral sclerosis and other neurogenic disorders. Muscle Nerve 21:336–344. doi: 10.1002/(SICI)1097-4598(199803)21:3<336:AID-MUS7>3.0CO;2-B PubMedCrossRefGoogle Scholar
  8. 8.
    Kleine BU, Stegeman DF, Schelhaas HJ, Zwarts MJ (2008) Firing pattern of fasciculations in ALS: evidence for axonal and neuronal origin. Neurology 70:353–359. doi: 10.1212/01.wnl.0000300559.14806.2a PubMedCrossRefGoogle Scholar
  9. 9.
    Kleine BU, Boekestein WA, Arts IMP, Zwarts MJ, Schelhaas HJ, Stegeman DF (2012) Fasciculations and their F-response revisited: high-density surface EMG in ALS and benign fasciculations. Clin Neurophysiol 123:399–405. doi: 10.1212/01.wnl.0000300559.14806.2a PubMedCrossRefGoogle Scholar
  10. 10.
    de Carvalho M, Swash M (2013) Fasciculation potentials and earliest changes in motor unit physiology in ALS. J Neurol Neurosurg Psychiatry 84:963–968. doi: 10.1136/jnnp-2012-304545 PubMedCrossRefGoogle Scholar
  11. 11.
    Hoff HE, Grant RS (1944) The supernormal period in the recovery cycle of motoneurons. J Neurophysiol 7:305–322Google Scholar
  12. 12.
    Calvin WH, Schwindt PC (1972) Steps in production of motoneuron spikes during rhythmic firing. J Neurophysiol 35:297–310PubMedGoogle Scholar
  13. 13.
    Kirkwood PA, Munson JB (1996) The incidence of initial doublets in the discharges of motoneurones of two different inspiratory muscles in the cat. J Physiol 493:577–587PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Kernell D (2006) The motoneurone and its muscle fibres. University Press, OxfordCrossRefGoogle Scholar
  15. 15.
    Denslow JS (1948) Double discharges in human motor units. J Neurophysiol 11:209–215PubMedGoogle Scholar
  16. 16.
    Kudina LP (1974) Double discharges of human motoneurons. Neirofiziologiya 6:119–124. doi: 10.1007/BF0062747 Google Scholar
  17. 17.
    Bawa P, Calancie B (1983) Repetitive doublets in human flexor carpi radialis muscle. J Physiol 339:123–132PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Garland SJ, Griffin L (1999) Motor unit double discharges: statistical anomaly or functional entity? Can J Appl Physiol 24:113–130. doi: 10.1139/h99-010 PubMedCrossRefGoogle Scholar
  19. 19.
    Kudina LP, Andreeva RE (2010) Repetitive doublet firing of motor units: evidence for plateau potentials in human motoneurones? Exp Brain Res 204:79–90. doi: 10.1007/s00221-010-2298-z PubMedCrossRefGoogle Scholar
  20. 20.
    Kudina LP, Andreeva RE (2013) Motoneuron double discharges: only one or two different entities? Front Cell Neurosci 7:75. doi: 10.3389/fncel.2013.00075 PubMedPubMedCentralGoogle Scholar
  21. 21.
    Kudina LP, Andreeva RE (2013) Delayed depolarization and firing behaviour of human motoneurons during voluntary muscle contractions. Front Hum Neurosci 7:793. doi: 10.3389/fnhum.2013.00793 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Piotrkiewicz M, Sebik O, Binboğa E, Młoźniak D, Kuraszkiewicz B, Tűrker KS (2013) Double discharges in human soleus muscle. Front Hum Neurosci 7:843. doi: 10.3389/fnhum.2013.00843 PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Harwood B, Rice CL (2014) Short interspike intervals and double discharges of anconeus motor unit action potentials for the production of dynamic elbow extensions. J Neurophysiol 111:2039–2046. doi:0.152/jn.00412.2013Google Scholar
  24. 24.
    Kudina LP, Churikova LI (1990) Testing excitability of human motoneurones capable of firing double discharges. Electroencephalogr Clin Neurophysiol 75:334–341. doi: 10.1016/0013-4694(90)90111-v PubMedCrossRefGoogle Scholar
  25. 25.
    Bawa P, Lemon R (1993) Recruitment of motor units in response to transcranial magnetic stimulation in man. J Physiol 471:445–464PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Kohara N, Kaji R, Kojima Y, Mills KR, Fujii H, Hamano T et al (1996) Abnormal excitability of the corticospinal pathway in patients with amyotrophic lateral sclerosis: a single motor unit study using transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol 101:32–41PubMedCrossRefGoogle Scholar
  27. 27.
    Weber M, Ferreira V, Eisen B (2009) Determinants of double discharges in amyotrophic lateral sclerosis and Kennedy disease. Clin Neurophysiol 120:1971–1977. doi: 10.1016/j.clinph.2009.08.011 PubMedCrossRefGoogle Scholar
  28. 28.
    Kudina LP, Andreeva RE (2014) Excitability properties of single human motor axons: are all axons identical? Front Cell Neurosci 8:75. doi: 10.3389/fncel.2014.00085 CrossRefGoogle Scholar
  29. 29.
    Partanen VSJ (1978) Double discharges in neuromuscular diseases. J Neurol Sci 36:377–382. doi: 10.1016/0022-510X(78)90045-X PubMedCrossRefGoogle Scholar
  30. 30.
    Rowiñska-Marciñska K, Zalewska E, Hausmanova-Petrusewicz I (1999) Double discharges of motor units in neuromuscular disorders. J Physiol (Paris) 93:175–182. doi: 10.1016/s0928-4257(99)80148-x CrossRefGoogle Scholar
  31. 31.
    Piotrkiewicz M, Kudina L, Mierzejewska J, Hausmanova-Petrusewicz I (2008) Analysis of double discharges in amyotrophic lateral sclerosis. Muscle Nerve 38:845–854. doi: 10.1002/mus.20997 PubMedCrossRefGoogle Scholar
  32. 32.
    Roth G (1980) Double discharges of distal origin: influence on the firing rhythm. J Neurol Sci 47:35–48PubMedCrossRefGoogle Scholar
  33. 33.
    Simpson JA (1969) Terminology of electromyography. Electroencephalogr Clin Neurophysiol 26:224–226PubMedCrossRefGoogle Scholar
  34. 34.
    Bergmans J (1970) The physiology of single human nerve fibres. Vander, LouvainGoogle Scholar
  35. 35.
    Bergmans J (1973) Physiological observations on single human nerve fibers. In: Desmedt JE (ed) New developments in electromyography and clinical neurophysiology, vol 2. Karger, Basel, pp 89–127Google Scholar
  36. 36.
    McNeil CJ, Butler JE, Taylor JL, Gandevia SC (2013) Testing the excitability of human motoneurons. Front Hum Neurosci 7:152. doi: 10.3389/fnhum.2013.00152 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Granit R, Kernell D, Smith RS (1963) Delayed depolarization and the repetitive response to intracellular stimulation of mammalian motoneurones. J Physiol 168:890–910PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Kernell D (1964) The delayed depolarization in cat and rat motoneurones. In: Eccles JC, Schade JP (eds) Progr Brain Res V.12. Elsevier, Amsterdam, pp 42–52CrossRefGoogle Scholar
  39. 39.
    Burke D, Kiernan MC, Bostock H (2001) Excitability of human axons. Clin Neurophysiol 112:1575–1585. doi: 10.1016/S1388-2457(01)00595-8 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 2015

Authors and Affiliations

  1. 1.Institute for Information Transmission Problems (Kharkevich Institute)Russian Academy of SciencesMoscowRussia

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