Article Data

  • Views 346
  • Dowloads 61

Original Research

Open Access

Topical Review: Modulation of Trigeminal Sensory Input in Humans: Mechanisms and Clinical Implications

  • Frank Lobbezoo1,*,
  • Mats Trulsson2
  • Reinhilde Jacobs3
  • Peter Svensson4
  • Samuel W. Cadden5
  • Daniel van Steenberghe6

1Department of Oral Function, Academic Centre for Dentistry Amsterdam (ACTA), Amsterdam, The Netherlands

2Karolinska Institutet, Department of Odontology, Huddinge, Sweden

3Research Council Flanders, Laboratory of Oral Physiology, School of Dentistry, Oral Pathology & Maxillo-Facial Surgery, Catholic University, Leuven, Belgium

4Center for Sensory-Motor Interaction, Orofacial Pain Laboratory, Aalborg University, Aalborg, Denmark

5The Dental School, University of Dundee, Dundee, Scotland

6School of Dentistry, Oral Pathology & Maxillo-Facial Surgery, Catholic University, Leuven, Belgium

DOI: 10.11607/jofph.16106 Vol.16,Issue 1,March 2002 pp.9-21

Published: 30 March 2002

*Corresponding Author(s): Frank Lobbezoo E-mail: f.lobbezoo@acta.nl

Abstract

In this review, the modulatory effects of tooth and implant loading, orofacial pain, and psychological factors on somatosensory and jaw-motor function in humans are assessed. Experimental studies on the control of jaw actions have revealed that patients with prostheses supported by osseointegrated implants show an impairment of fine motor control of the mandible. One possibility is that this may be related to the loss of afferent information from periodontal ligament mechanoreceptors, which results in considerably higher and more variable forces to hold and manipulate food between the teeth. However, psychophysical investigations have shown that patients still perceive mechanical stimuli exerted on osseointegrated implants in the jawbone. The use of somatosensory evoked potentials may reveal what specific receptor groups are responsible for this so-called osseoperception phenomenon. Orofacial pain is another modulator of trigeminal system functioning. Experimental jaw muscle pain has several effects on the somatosensory and motor function of the masticatory system, all of them serving to warn the individual about the ongoing damaging of tissues. Finally, the influence of mental state on the sensory and motor functions of the trigeminal system will be addressed. While some animal studies suggest that psychological stress can reduce acute pain, less speculative are the findings in human subjects that the anticipation of receiving a painful stimulus or undertaking difficult mental tasks can modulate jaw reflexes, including those evoked by mechanical stimuli applied to the teeth. Since such stimuli occur regularly during normal oral activities, the study of the resulting motor effects may yield clinically meaningful results in the context of other variables that modulate mandibular function.


Keywords

trigeminal system; modulation; somatosensory function; jaw-motor function; pain

Cite and Share

Frank Lobbezoo,Mats Trulsson,Reinhilde Jacobs,Peter Svensson,Samuel W. Cadden,Daniel van Steenberghe. Topical Review: Modulation of Trigeminal Sensory Input in Humans: Mechanisms and Clinical Implications . Journal of Oral & Facial Pain and Headache. 2002. 16(1);9-21.

References

1. Linden RA, Millar BJ. The response characteristics of mechanoreceptors related to their position in the cat periodontal ligament. Arch Oral Biol 1988;33:51–56.

2. van Steenberghe D, van den Bergh A, De Vries JH, Schoo WH. The influence of advanced periodontitis on the psychophysical threshold level of periodontal mechanoreceptors in man. J Periodont Res 1981;16:199–204.

3. Trulsson M, Johansson RS. Encoding of tooth loads by human periodontal afferents and their role in jaw motor control. Prog Neurobiol 1996;49:267–284.

4. Johansson RS, Olsson KÅ. Microelectrode recordings from human oral mechanoreceptors. Brain Res 1976;118:307–311.

5. Trulsson M, Johansson RS, Olsson KÅ. Directional sensitivity of human periodontal mechanoreceptive afferents to forces applied to the teeth. J Physiol (London) 1992; 447:373–389.

6. Sakada S, Kamio E. Receptive fields and directional sensitivity of single sensory units innervating the periodontal ligamentsof the cat mandibular teeth. Bull Tokyo Dent Coll 1971;12:25–43.

7. Karita K, Tabata T. Response fields of the periodontal mechanosensitive units in the superior alveolar nerve of the cat. Exp Neurol 1985;90:558–565.

8. Hannam AG. Receptor fields of periodontal mechanosensitive units in the dog. Arch Oral Biol 1970;15: 971–978.

9. Trulsson M. Multiple-tooth receptive fields of single human periodontal mechanoreceptive afferents. J Neurophysiol 1993;69:474–481.

10. Trulsson M, Johansson RS. Encoding of amplitude and rate of forces applied to the teeth by human periodontal mechanoreceptive afferents. J Neurophysiol 1994;72: 1734–1744.

11. Trulsson M, Johansson RS. Forces applied by the incisors and roles of periodontal afferents during food-holding and

- biting tasks. Exp Brain Res 1996;107:486–496.

12. Trulsson M, Gunne HS. Food-holding and -biting behavior in human subjects lacking periodontal receptors. J Dent Res 1998;77:574–582.

13. Jacobs R, van Steenberghe D. Role of periodontal ligament receptors in the tactile function of teeth: A review. J Periodont Res 1994;29:153–167.

14. Jacobs R. Neurological versus psychophysical assessment of osseoperception. In: Jacobs R (ed). Osseoperception. Leuven: Department of Periodontology, KU Leuven, 1998:75–88.

15. Brånemark P-I. Osseointegration: biotechnological perspective and clinical modality. In: Brånemark P-I, Rydevik BL, Skalak R (eds). Osseointegration in Skeletal Reconstruction and Joint Replacement. Chicago: Quintessence Publishing Co, Inc, 1997:1–24.

16. Jacobs R, van Steenberghe D. Comparative evaluation of the oral tactile function by means of teeth or implant-supported prostheses. Clin Oral Implants Res 1991;2: 75–80.

17. Jacobs R, van Steenberghe D. Comparison between implant-supported prostheses and teeth regarding the passive threshold level. Int J Oral Maxillofac Implants 1993;8:549–554.

18. Sakada S. Physiology of mechanical senses of the oral structure. In: Kawamura Y (ed). Frontiers of Oral Physiology, vol 4. Basel: Karger, 1983:1–32.

19. Wang YH, Kojo T, Ando H, et al. Nerve regeneration after implantation in peri-implant area: A histiological study on different implant materials in dogs. In: Jacobs R (ed). Osseoperception. Leuven: KU Leuven, 1998:75–88.

20. Bonte B, Linden RW, Scott BJ, van Steenberghe D. Role of periodontal mechanoreceptors in evoking reflexes in the jaw-closing muscles of the cat. J Physiol (London) 1993;465:581–594.

21. Jacobs R, van Steenberghe D. Qualitative evaluation of the masseteric poststimulus EMG complex following mechanical or acoustic stimulation of osseointegrated oral implants. Int J Oral Maxillofac Implants 1995;10: 175–182.

22. Van Loven K, Jacobs R, Swinnen A, Van Huffel S, Van Hees J, van Steenberghe D. Sensations and trigeminal somatosensory-evoked potentials elicited by electrical stimulation of endosseous oral implants in humans. Arch Oral Biol 2000;45:1083–1090.

23. Crombie IK , Croft PR, Linton SJ, LeResche L, Von Korff M (eds). Epidemiology of Pain: A Report of the Task Force on Epidemiology of the International Association for the Study of Pain. Seattle: IASP, 1999.

24. Svensson P, Jensen K. Human studies of experimental pain from muscle. In: Olesen J, Tfelt-Hansen P, Welch KMA (eds). The Headaches. Philadelphia: Lippincott-Williams & Wilkins, 2000 (2nd ed):565–571.

25. Stohler CS. Craniofacial pain and motor function: Pathogenesis, clinical correlates, and implications. Crit Rev Oral Biol Med 1999;10:504–518.

26. Sessle BJ. Acute and chronic craniofacial pain: Brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000;11:57–91.

27. Kellgren JH. Observations on referred pain arising from muscle. Clin Sci (London) 1938;3:175–190.

28. Mense S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain 1993;54:241–289.

29. Stohler CS, Zhang X, Ashton-Miller JA. An experimental model of jaw muscle pain in man. In: Davidovitch Z (ed). The Biological Mechanisms of Tooth Movement and Craniofacial Adaptation. Columbus: Ohio State University, College of Dentistry, 1992:503–511.

30. Svensson P, Graven-Nielsen T, Arendt-Nielsen L. Mechanical hyperesthesia of human facial skin induced by tonic painful stimulation of jaw muscles. Pain 1998;74:93–100.

31. Stohler CS, Kowalski CJ. Spatial and temporal summation of sensory and affective dimensions of deep somatic pain. Pain 1999;79:165–173.

32. 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.

33. Travell JG, Simons DG. Myofascial Pain and Dysfunction: The Trigger Point Manual. Baltimore: Williams & Wilkins, 1983.

34. Hutchins HC, Reynolds OE. Experimental investigation of the referred pain of aerodontalgia. J Dent Res 1947; 26:3–8.

35. Ren K, Dubner R. Central nervous system plasticity and persistent pain. J Orofac Pain 1999;13:155–163.

36. Sessle BJ. The neural basis of temporomandibular joint and masticatory muscle pain. J Orofac Pain 1999;13:238–245.

37. Sörensen J, Graven-Nielsen T, Henriksson K-G, Bengtsson M, Arendt-Nielsen L. Hyperexcitability in fibromyalgia. J Rheumatol 1998;25:152–155.

38. Koelbaek JM, Graven-Nielsen T, Schou-Olesen A, Arendt-Nielsen L. Generalised muscular hyperalgesia in chronic whiplash syndrome. Pain 1999;83:229–234.

39. Svensson P, List T, Hector G. Analysis of stimulus-evoked pain in patients with myofascial temporomandibular pain disorders. Pain 2001;92:399–409.

40. Laursen RJ, Graven-Nielsen T, Jensen TS, Arendt-Nielsen

L. The effect of compression and regional anaesthetic block on referred pain intensity in humans. Pain 1999;80:257–263.

41. Cairns BE, Hu JW, Arendt-Nielsen L, Sessle BJ, Svensson

P. Sex-related differences in human pain perception and rat afferent discharge evoked by injection of glutamate into the masseter muscle. J Neurophysiol 2001;86: 782–791.

42. Dao TT, LeResche L. Gender differences in pain. J Orofac Pain 2000;14:169–184.

43. 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.

44. Stohler CS, Zhang X, Lund JP. The effect of experimental jaw muscle pain on postural muscle activity. Pain 1996;66:215–221.

45. 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.

46. Hu JW, Yu X-M, Vernon H, Sessle BJ. Excitatory effects on neck and jaw muscle activity of inflammatory irritant applied to cervical paraspinal tissues. Pain 1993; 55:243–250.

47. Yu XM, Sessle BJ, Vernon H, Hu JW. Effects of inflammatory irritant application to the rat temporomandibular joint on jaw and neck muscle activity. Pain 1995;60: 143–149.

48. Wang K, Arima T, Arendt-Nielsen L, Svensson P. EMG-force relationships are influenced by experimental jaw-muscle pain. J Oral Rehabil 2000;27:394–402.

49. 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.

50. Westberg KG, Clavelou P, Schwartz G, Lund JP. Effects of chemical stimulation of masseter muscle nociceptors on trigeminal motoneuron and interneuron activities during fictive mastication in the rabbit. Pain 1997;73: 295–308.

51. Amit Z, Galina ZH. Stress-induced analgesia: Adaptive pain suppression. Physiol Rev 1986; 66: 1091–1120.

52. Vassel A, Pajot J, Aigouy L, Rajona J, Woda A. Effects, in the rat, of various stressing procedures on the jaw-opening reflex induced by tooth-pulp stimulation. Arch Oral Biol 1986; 31:159–163.

53. Bathien N. Réflexes spinaux chez l’homme et niveau d’attention. [Human spinal reflexes and attention levels.] Electroencephalogr Clin Neurophysiol 1971;30:32–37.

54. Hugelin A. Bodily changes during arousal, attention, and emotion. In: Hockman CH (ed). Limbic System Mechanisms and Autonomic Function. Springfield, IL: CC Thomas, 1972:202–218.

55. Willer JC. Anticipation of pain-produced stress: Electrophysiological study in man. Physiol Behav 1980;25:49–51.

56. Willer JC, Boureau F, Albe-Fessard D. Supraspinal influences on nociceptive flexion reflex and pain sensation in man. Brain Res 1979;179:61–68.

57. Willer JC, Dehen H, Cambier J. Stress induced analgesia in humans: Endogenous opioids and naloxone reversible depression of pain reflexes. Science 1981;212: 689–691.

58. Orchardson R, Cadden SW. Mastication. In: Linden RWA (ed). Frontiers of Oral Biology, Volume 9: The Scientific Basis of Eating. Basel; New York: Karger, 1998:76–121.

59. Yu SK, Schmitt A, Sessle BJ. Inhibitory effects on jaw muscle activity of innocuous and noxious stimulation of facial and intraoral sites in man. Arch Oral Biol 1973;18:861–870.

60. Cadden SW, Newton JP. A comparison of reflex depressions of activity in jaw-closing muscles evoked by intra-and peri-oral stimuli in man. Arch Oral Biol 1988;33:863–869.

61. Scott AJ, Cadden SW. Suppression of an inhibitory jaw reflex by the anticipation of pain in man. Pain 1996; 66:125–131.

62. Cadden SW, Newton JP. The effects of attentional factors on an inhibitory jaw reflex in man. Exp Physiol 1995;80:299–305.

63. Cadden SW, van der Glas HW, Lobbezoo F, van der Bilt

A. The influence of attentional factors on short- and longlatency jaw reflexes in man. Arch Oral Biol 1996; 41:995–998.

64. van der Glas HW, De Laat A, van Steenberghe D. Oral pressure receptors mediate a series of inhibitory and excitatory periods in the masseteric post-stimulus EMG complex following tapping of a tooth in man. Brain Res 1985;337:117–125.

65. van der Glas HW, Abbink JH, van der Bilt A, Cadden SW. Analysis of differences between conditioned and control reflex series in EMG recordings. J Neurosci Methods 1995;58:117–125.

66. van der Glas HW, Cadden SW, van der Bilt A. Mechanisms underlying the effects of remote noxious stimulation and mental activities on exteroceptive jaw reflexes in man. Pain 2000;84:193–202.

67. Wang K, Svensson P, Arendt-Nielsen L. Modulation of exteroceptive suppression periods in human jaw-closing muscles by local and remote experimental muscle pain. Pain 1999;82:253–262.

68. Cadden SW, Newton JP. The effects of inhibitory controls triggered by heterotopic noxious stimuli on a jaw reflex evoked by perioral stimuli in man. Arch Oral Biol 1994;39:473–480.

69. Cadden SW, van der Glas HW, Lobbezoo F, van der Bilt

A. Effects of remote noxious stimulation on exteroceptive reflexes in human jaw-closing muscles. Brain Res 1996;726:189–197.

70. Maillou P, Cadden SW. Effects of remote deep somatic noxious stimuli on a jaw reflex in man. Arch Oral Biol 1997;42:323–327.

71. Newton JP, Cadden SW. Dissociation of jaw reflex modulation and pain from thermal stimuli. J Dent Res 1998;77:1006.

72. Le Bars D, Villanueva L, Bouhassira D, Willer JC. Diffuse noxious inhibitory controls (DNIC) in animals and in man. Patol Fiziol Eksp Ter 1992; Jul–Aug:55–65.

73. De Laat A, van der Glas HW, Weytjens JL, van Steenberghe D. The masseteric post-stimulus electromyographic-complex in people with dysfunction of the mandibular joint. Arch Oral Biol 1985;30:177–180.

74. Schoenen J, Jamart B, Gerard P, Lenarduzzi P, Delwaide PJ. Exteroceptive suppression of temporalis muscle activity in chronic headache. Neurology 1987;37: 1834–1836.

75. De Laat A, Svensson P, Macaluso GM. Are jaw and facial reflexes modulated during clinical or experimental orofacial pain? J Orofac Pain 1998;12:260–271.

76. McCreary CP, Clark GT, Merril RL, Flack V, Oakley ME. Psychological distress and diagnostic subgroups of temporomandibular disorder patients. Pain 1991;44: 29–34.

77. Slager GE, Otten E, Nagashima T, van Willigen JD. The riddle of the large loss in bite force after fast jaw-closing movements. J Dent Res 1998;77:1684–1693.

78. Appenteng K, Curtis JC, Grimwood P, Min MY, Yang HW. Modulation of transmission in reflex pathways of trigeminal motoneurones. In: Taylor A, Gladden MH, Durbaba R (eds). Alpha and Gamma Motor Systems. New York: Plenum, 1995:29–36.

79. Davidoff RA. Skeletal muscle tone and the misunderstood stretch reflex. Neurology 1992;42:951–963.

80. Passatore M, Grassi C, Filippi GM. Sympathetically-induced development of tension in jaw muscles: The possible contraction of intrafusal muscle fibres. Pflügers Arch 1985;405:297–304.

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