Article Data

  • Views 263
  • Dowloads 24

Original Research

Open Access

Changes in Human Primary Motor Cortex Activity During Acute Cutaneous and Muscle Orofacial Pain

  • Paul G. Nash2
  • Vaughan G. Macefield3
  • Iven J. Klineberg4
  • Sylvia M. Gustin1
  • Greg M. Murray
  • Luke A. Henderson1,*,

1Univ Sydney, Fac Dent, Dept Anat & Histol, Sydney, NSW 2006, Australia

2Stanford Sch Med, Syst Neurosci & Pain Lab, Dept Anesthesia, Stanford, CA USA

3Univ Western Sydney, Sch Med, Sydney, NSW, Australia

4Univ Sydney, Nobel Biocare Chair Oral Rehabil, Jaw Funct & Orofacial Pain Res Unit, Fac Dent, Sydney, NSW 2006, Australia

DOI: 10.11607/jofph.24.4.07 Vol.24,Issue 4,December 2010 pp.379-390

Published: 30 December 2010

*Corresponding Author(s): Luke A. Henderson E-mail: lukeh@anatomy.usyd.edu.au

Abstract

Aims: To use functional magnetic resonance imaging (fMRI) to determine whether orofacial cutaneous or muscle pain is associated with changes in primary motor cortex (M1) activity that outlast the duration of perceived pain, and whether these M1 changes are different during cutaneous pain compared with muscle pain. Methods: fMRI was used in healthy subjects experiencing orofacial muscle (n = 17) or cutaneous (n = 15) pain induced by bolus injections of hypertonic saline (4.5%) into the belly of the masseter muscle (0.5 ml) or subcutaneously (0.2 ml) into the overlying skin, respectively. To determine the effects of the injection volume, isotonic saline (n = 4) was injected into the masseter muscle. Results: Similar pain scores were observed following subcutaneous (mean [± SEM]; 4.73 ± 0.51) or intramuscular injections (4.35 ± 0.56). Orofacial muscle but not cutaneous pain was associated with a transient increase in signal intensity in the contralateral M1. Cutaneous and muscle orofacial pains were associated with similar signal intensity decreases within the contralateral M1 that continued to decrease for the entire scanning period. Isotonic saline did not evoke pain or changes in M1 signal intensity. Conclusion: The transient contralateral M1 signal intensity increase during orofacial muscle pain may underlie escape-like motor patterns. However, once the initial threat has subsided, longerterm reductions in M1 activity and/or excitability may occur to aid in minimizing movement of the affected part, an effect consistent with the general proposals of the Pain Adaptation Model.

Keywords

face;jaw muscle;magnetic resonance imaging (MRI);pain;skin;trigeminal

Cite and Share

Paul G. Nash,Vaughan G. Macefield,Iven J. Klineberg,Sylvia M. Gustin,Greg M. Murray,Luke A. Henderson. Changes in Human Primary Motor Cortex Activity During Acute Cutaneous and Muscle Orofacial Pain. Journal of Oral & Facial Pain and Headache. 2010. 24(4);379-390.

References

1. Bandler R, Price JL, Keay KA. Brain mediation of active and passive emotional coping. Prog Brain Res 2000;122: 333–349.

2. Johansson H, Sojka P. Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: A hypothesis. Med Hypothes 1991;35: 196 –203.

3. Appelberg B, Hulliger M, Johansson H, Sojka P. Actions on gammamotoneurones elicited by electrical stimulation of group III muscle afferent fibres in the hind limb of the cat. J Physiol 1983;335:275–292.

4. Thunberg J, Ljubisavljevic M, Djupsjobacka M, Johans-son H. Effects on the fusimotor-muscle spindle system induced by intramuscular injections of hypertonic saline. Exp Brain Res 2002;142:319–326.

5. Johansson H, Sjolander P, Sojka P. Fusimotor effects in triceps surae muscle elicited by natural and electrical stimulation of joint afferents. Neuro Orthoped 1988;6:67–80.

6. Johansson H, Sjolander P, Sojka P, Wadell I. Reflex actions on the gammamuscle spindle systems of muscles acting at the knee joint elicited by stretch of the posterior cruciate ligament. Neuro Orthoped 1989;8:9–21.

7. Birznieks I, Burton AR, Macefield VG. The effects of experimental muscle and skin pain on the static stretch sensitivity of human muscle spindles in relaxed leg muscles. J Physiol 2008;586:2713–2723.

8. Birznieks I, Burton AR, Macefield VG. Does muscle pain increase muscle stiffness? Physiol News 2008;73:21–22.

9. Simons DG, Mense S. Understanding and measurement of muscle tone as related to clinical muscle pain. Pain 1998;75:1–17.

10. Svensson P, Graven-Nielsen T, Matre D, Arendt-Nielsen L. Experimental muscle pain does not cause long-lasting increases in resting electromyographic activity. Muscle Nerve 1998;21:1382–1389.

11. Lund JP, Donga R, Widmer CG, Stohler CS. The pain-adaptation model: A discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 1991;69:683–694.

12. Graven-Nielsen T, Svensson P, Arendt-Nielsen L. Effects of experimental muscle pain on muscle activity and coordination during static and dynamic motor function. Electroenceph Clin Neurophysiol 1997;105:156–164.

13. Svensson P, Arendt-Nielsen L, Houe L. Sensory-motor interactions of human experimental unilateral jaw muscle pain: A quantitative analysis. Pain 1996;64:241–249.

14. Svensson P, Wang K, Sessle BJ, Arendt-Nielsen L. Associations between pain and neuromuscular activity in the human jaw and neck muscles. Pain 2004;109:225–232.

15. Murray GM, Peck CC. Orofacial pain and jaw muscle activity: A new model. J Orofac Pain 2007;21:263–278.

16. Matre DA, Sinkjaer T, Svensson P, Arendt-Nielsen L. Experimental muscle pain increases the human stretch reflex. Pain 1998;75:331–339.

17. Sohn MK, Graven-Nielsen T, Arendt-Nielsen L, Svensson

P. Inhibition of motor unit firing during experimental muscle pain in humans. Muscle Nerve 2000;23:1219–1226.

18. Svensson P, Macaluso GM, De Laat A, Wang K. Effects of local and remote muscle pain on human jaw reflexes evoked by fast stretches at different clenching levels. Exp Brain Res 2001;139:495–502.

19. Adachi K, Murray GM, Lee JC, Sessle BJ. Noxious lingual stimulation influences the excitability of the face primary motor cerebral cortex (face MI) in the rat. J Neurophysiol 2008;100:1234–1244.

20. Farina S, Valeriani M, Rosso T, et al. Transient inhibition of the human motor cortex by capsaicin-induced pain. A study with transcranial magnetic stimulation. Neurosci Lett 2001;314:97–101.

21. Le Pera D, Graven-Nielsen T, Valeriani M, et al. Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 2001;112: 1633–1641.

22. Halkjaer L, Melsen B, McMillan AS, Svensson P. Influence of sensory deprivation and perturbation of trigeminal afferent fibers on corticomotor control of human tongue musculature. Exp Brain Res 2006;170:199–205.

23. Romaniello A, Cruccu G, McMillan AS, Arendt-Nielsen L, Svensson P. Effect of experimental pain from trigeminal muscle and skin on motor cortex excitability in humans. Brain Res 2000;882:120–127.

24. Boudreau S, Romaniello A, Wang K, Svensson P, Sessle BJ, Arendt-Nielsen L. The effects of intraoral pain on motor cortex neuroplasticity associated with short-term novel tongue-protrusion training in humans. Pain 2007;132: 169–178.

25. Dubner R, Ren K. Brainstem mechanisms of persistent pain following injury. J Orofac Pain 2004;18:299–305.

26. Yu XM, Sessle BJ, Hu JW. Differential effects of cutaneous and deep application of inflammatory irritant on mechanoreceptive field properties of trigeminal brain stem nociceptive neurons. J Neurophysiol 1993;70:1704–1707.

27. Henderson LA, Bandler R, Gandevia SC, Macefield VG. Distinct forebrain activity patterns during deep versus superficial pain. Pain 2006;120:286–296.

28. Kupers RC, Svensson P, Jensen TS. Central representation of muscle pain and mechanical hyperesthesia in the orofacial region: A positron emission tomography study. Pain 2004;108:284–293.

29. Melzack R. The McGill pain questionnaire: Major properties and scoring methods. Pain 1975;1:277–299.

30. Borg G, Holmgren A, Lindblad I. Quantitative evaluation of chest pain. Acta Med Scand 1981;644:43–45.

31. Nash PG, Macefield VG, Klineberg IJ, Murray GM, Henderson LA. Differential activation of the human trigeminal nuclear complex by noxious and nonnoxious orofacial stimulation. Hum Brain Mapp 2009;30:3772–3782.

32. Friston KJ, Holmes AP, Worsley K, Poline JB, Frith CD, Frackowiak RS. Statistic parametric maps in functional imaging: A general linear approach. Hum Brain Mapp 1995; 2:189–210.

33. Casey KL. Forebrain mechanisms of nociception and pain: Analysis through imaging. Proc Nat Acad Sci USA 1999; 96:7668–7674.

34. Moulton EA, Keaser ML, Gullapalli RP, Greenspan JD. Regional intensive and temporal patterns of functional MRI activation distinguishing noxious and innocuous contact heat. J Neurophysiol 2005;93:2183–2193.

35. Svensson P, Minoshima S, Beydoun A, Morrow TJ, Casey KL. Cerebral processing of acute skin and muscle pain in humans. J Neurophysiol 1997;78:450–460.

36. Timmermann L, Ploner M, Haucke K, Schmitz F, Baltissen R, Schnitzler A. Differential coding of pain intensity in the human primary and secondary somatosensory cortex. J Neurophysiol 2001;86:1499–1503.

37. Porro CA, Cettolo V, Francescato MP, Baraldi P. Temporal and intensity coding of pain in human cortex. J Neurophysiol 1998;80:3312–3320.

38. Naito E, Roland PE, Ehrsson HH. I feel my hand moving: A new role of the primary motor cortex in somatic perception of limb movement. Neuron 2002;36:979–988.

39. Schieppati M. The Hoffmann reflex: A means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 1987;28:345–376.

40. Shulman RG, Rothman DL, Hyder F. A BOLD search for baseline. NeuroImage 2007;36:277–281.

41. Smith AJ, Blumenfeld H, Behar KL, Rothman DL, Shulman RG, Hyder F. Cerebral energetics and spiking frequency: The neurophysiological basis of fMRI. Proc Nat Acad Sci USA 2002;99:10765–10770.

42. Schridde U, Khubchandani M, Motelow JE, Sanganahalli BG, Hyder F, Blumenfeld H. Negative BOLD with large increases in neuronal activity. Cereb Cortex 2008;18: 1814–1827.

43. Shmuel A, Augath M, Oeltermann A, Logothetis NK. Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 2006;9:569–577.

44. Shmuel A, Yacoub E, Pfeuffer J, et al. Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 2002;36:1195–1210.

45. Sae-Lee D, Whittle T, Forte AR, et al. Effects of experimen-tal pain on jaw muscle activity during goal-directed jaw movements in humans. Exp Brain Res 2008;189:451–462.

Abstracted / indexed in

Science Citation Index (SCI)

Science Citation Index Expanded (SCIE)

BIOSIS Previews

Scopus

Cumulative Index to Nursing and Allied Health Literature (CINAHL)

Submission Turnaround Time

Conferences

Top