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Effects of sympathetic stimulation on the rhythmical jaw movements produced by electrical stimulation of the cortical masticatory areas of rabbits

Experimental Brain Research volume 162, pages 14–22 (2005)Cite this article

Abstract

The somatomotor and sympathetic nervous systems are intimately linked. One example is the influence of peripheral sympathetic fibers on the discharge characteristics of muscle spindles. Since muscle spindles play important roles in various motor behaviors, including rhythmic movements, the working hypothesis of this research was that changes in sympathetic outflow to muscle spindles can change rhythmic movement patterns. We tested this hypothesis in the masticatory system of rabbits. Rhythmic jaw movements and EMG activity induced by long-lasting electrical cortical stimulation were powerfully modulated by electrical stimulation of the peripheral stump of the cervical sympathetic nerve (CSN). This modulation manifested itself as a consistent and marked reduction in the excursion of the mandibular movements (often preceded by a transient modest enhancement), which could be attributed mainly to corresponding changes in masseter muscle activity. These changes outlasted the duration of CSN stimulation. In some of the cortically evoked rhythmic jaw movements (CRJMs) changes in masticatory frequency were also observed. When the jaw-closing muscles were subjected to repetitive ramp-and-hold force pulses, the CRMJs changed characteristics. Masseter EMG activity was strongly enhanced and digastric EMG slightly decreased. This change was considerably depressed during CSN stimulation. These effects of CSN stimulation are similar in sign and time course to the depression exerted by sympathetic activity on the jaw-closing muscle spindle discharge. It is suggested that the change in proprioceptive information induced by an increase in sympathetic outflow (a) has important implications even under normal conditions for the control of motor function in states of high sympathetic activity, and (b) is one of the mechanisms responsible for motor impairment under certain pathological conditions such as chronic musculoskeletal head-neck disorders, associated with stress conditions.

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References

  • Bowman WC (1981) Effects of adrenergic activators and inhibitors on the skeletal muscles. In: Szekeres L (ed) Handbook of experimental pharmacology, Adrenergic activators and inhibitor. Springer, Berlin Heidelberg New York, pp 47–128

  • Cash RM, Linden RWA (1982) Effects of sympathetic nerve stimulation on intra-oral mechanoreceptor activity in the cat. J Physiol (Lond) 329:451–463

    Google Scholar 

  • Dorward PK, Burke SL, Janig W, Cassell J (1987) Reflex responses to baroreceptor, chemoreceptor and nociceptor inputs in single renal sympathetic neurones in the rabbit and the effects of anaesthesia on them. J Auton Nerv Syst 18:39–54

    Article  CAS  PubMed  Google Scholar 

  • Eldred E, Schnitzlein H, Buchwald J (1960) Response of muscle spindles to stimulation of the sympathetic trunk. Exp Neurol 2:13–25

    Article  CAS  PubMed  Google Scholar 

  • Goodwin GM, Luschei ES (1974) Effects of destroying spindle afferents from jaw muscles on mastication in monkeys. J Neurophysiol 37:967–981

    CAS  PubMed  Google Scholar 

  • Grassi C, Deriu F, Artusio E, Passatore M (1993a) Modulation of the jaw jerk reflex by the sympathetic nervous system. Arch Ital Biol 131:213–226

    CAS  PubMed  Google Scholar 

  • Grassi C, Deriu F, Passatore M (1993b) Effect of sympathetic nervous system activation on the tonic vibration reflex in rabbit jaw closing muscles. J Physiol (Lond) 469:601–613

    Google Scholar 

  • Grassi C, Deriu F, Roatta S, Santarelli R, Azzena GB, Passatore M (1996) Sympathetic control of skeletal muscle function: possible co-operation between noradrenaline and neuropeptide Y in rabbit jaw muscles. Neurosci Lett 212:204–208

    Article  CAS  PubMed  Google Scholar 

  • Hellström, F, Thundberg J, Roatta S, Djupsjöbaka M, Johansson H (2002) Responses of muscle spindles in dorsal neck muscles during stimulation of the cervical sympathetic nerve at frequencies within the physiological range. Ph.D. Thesis, Umea University

  • Hidaka O, Morimoto T, Masuda Y, Kato T, Matsuo R, Inoue T, Kobayashi M, Takada K (1997) Regulation of masticatory force during cortically induced rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol 77:3168–3179

    CAS  PubMed  Google Scholar 

  • Hidaka O, Morimoto T, Kato T, Masuda Y, Inoue T, Takada K (1999) Behavior of jaw muscle spindle afferents during cortically induced rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol 82:2633–2640

    CAS  PubMed  Google Scholar 

  • Hunt CC (1960) The effect of sympathetic stimulation on mammalian muscle spindles. J Physiol (Lond) 151:332–341

    Google Scholar 

  • Kendrick E, Oberg B, Wennergren G (1972) Vasoconstrictor fibre discharge to skeletal muscle, kidney, intestine and skin at varying levels of arterial baroreceptor activity in the cat. Acta Physiol Scand 85:464–76

    CAS  PubMed  Google Scholar 

  • Komuro A, Morimoto T, Iwata K, Inoue T, Masuda Y, Kato T, Hidaka O (2001) Putative feed-forward control of jaw-closing muscle activity during rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol 86:2834–2844

    CAS  PubMed  Google Scholar 

  • Liu ZJ, Masuda Y, Inoue T, Fuchihata H, Sumida A, Takada K, Morimoto T (1993) Coordination of cortically induced rhythmic jaw and tongue movements in the rabbit. J Neurophysiol 69:569–584

    CAS  PubMed  Google Scholar 

  • Lund JP, Sasamoto K, Murakami T, Olsson KA (1984) Analysis of rhythmical jaw movements produced by electrical stimulation of motor-sensory cortex of rabbits. J Neurophysiol 52:1014–1029

    CAS  PubMed  Google Scholar 

  • Matsuo R, Ikehara A, Nokubi T, Morimoto T (1995) Inhibitory effect of sympathetic stimulation on activities of masseter muscle spindles and the jaw jerk reflex in rats. J Physiol (Lond) 483:239–250

    Google Scholar 

  • Mellander S, Johansson B (1968) Control of resistance, exchange, and capacitance functions in the peripheral circulation. Pharmacol Rev 20:117–196

    CAS  PubMed  Google Scholar 

  • Morimoto T, Inoue T, Masuda Y, Nagashima T (1989) Sensory components facilitating jaw-closing muscle activities in the rabbit. Exp Brain Res 76:424–440

    CAS  PubMed  Google Scholar 

  • Passatore M, Filippi GM (1983) Sympathetic modulation of periodontal mechanoreceptors. Arch Ital Biol 121:55–65

    CAS  PubMed  Google Scholar 

  • Passatore M, Deriu F, Grassi C, Roatta S (1996) A comparative study of changes operated by sympathetic nervous system activation on spindle afferent discharge and on tonic vibration reflex in rabbit jaw muscles. J Auton Nerv Syst 57:163–167

    Article  CAS  PubMed  Google Scholar 

  • Ribbers GM, Mulder T, Geurts AC, den Otter RA (2002) Reflex sympathetic dystrophy of the left hand and motor impairments of the unaffected right hand: impaired central motor processing? Arch Phys Med Rehabil 83:81–85

    Article  PubMed  Google Scholar 

  • Rissen D, Melin B, Sandsjo L, Dohns I, Lundberg U (2000) Surface EMG and psychophysiological stress reactions in women during repetitive work. Eur J Appl Physiol 83:215–222

    Article  CAS  PubMed  Google Scholar 

  • Roatta S, Deriu F, Artusio E, Passatore M (1996) A simple, non-invasive and inexpensive method for evaluating the displacement of local tissue surfaces: from vascular changes to muscle contraction. Clin Physiol 16:83–94

    CAS  PubMed  Google Scholar 

  • Roatta S, Windhorst U, Ljubisavljevic M, Johansson H, Passatore M (2002) Sympathetic modulation of muscle spindle afferent sensitivity to stretch in rabbit jaw closing muscles. J Physiol (Lond) 540:237–248

    Google Scholar 

  • Schwartzman RJ, Kerrigan J (1990) The movement disorder of reflex sympathetic dystrophy. Neurology 40:57–61

    CAS  PubMed  Google Scholar 

  • Sjogaard G, Lundberg U, Kadefors R (2000) The role of muscle activity and mental load in the development of pain and degenerative processes at the muscle cell level during computer work. Eur J Appl Physiol 83:99–105

    Article  CAS  PubMed  Google Scholar 

  • Turker KS (2002) Reflex control of human jaw muscles. Crit Rev Oral Biol Med 13:85–104

    PubMed  Google Scholar 

  • Turker KS, Jenkins M (2000) Reflex responses induced by tooth unloading. J Neurophysiol 84:1088–1092

    PubMed  Google Scholar 

  • Weijs WA, Korfage JA, Langenbach GJ (1989) The functional significance of the position of the centre of rotation for jaw opening and closing in the rabbit. J Anat 162:133–148

    CAS  PubMed  Google Scholar 

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Acknowledgements

The research was supported by the Italian Ministry of Scientific Research (MIUR) and by Center for Musculoskeletal Research, Umea, University of Gavle. S.L. was supported by a fellowship from the Center for Musculoskeletal Research, Umea, University of Gavle.

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Affiliations

  1. Physiology Division, Department of Neuroscience, Medical School, University of Turin, c.so Raffaello 30, 10125, Turin, Italy

    S. Roatta & M. Passatore

  2. Center for Musculoskeletal Research, University of Gävle, Umeå, Sweden

    U. Windhorst, M. Djupsjöbacka & S. Lytvynenko

  3. Zentrum Neuro- and Pathophysiologie, Universität Göttingen, Göttingen, Germany

    U. Windhorst

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  1. S. Roatta
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  2. U. Windhorst
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  3. M. Djupsjöbacka
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  4. S. Lytvynenko
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  5. M. Passatore
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Correspondence to S. Roatta.

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Roatta, S., Windhorst, U., Djupsjöbacka, M. et al. Effects of sympathetic stimulation on the rhythmical jaw movements produced by electrical stimulation of the cortical masticatory areas of rabbits. Exp Brain Res 162, 14–22 (2005). https://doi.org/10.1007/s00221-004-2102-z

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  • DOI: https://doi.org/10.1007/s00221-004-2102-z

Keywords

  • Sympathetic nervous system
  • Muscle spindle
  • Mastication
  • Motor control