From Movement to Pain: A Tribute to Professor James P. Lund

This tribute article to Professor James P. Lund stems from 6 of the presentations delivered at the July 1, 2008, symposium that honored 3 “giants” in orofacial neuroscience: B.J. Sessle, A.G. Hannam, and J.P. Lund. It was noted that soon after his training as a dentist in Australia, Jim Lund became interested in research. At the time he decided to do a PhD, there was a lot of discussion about how rhythmic movements were programmed. The early belief, based on Sherrington’s studies of motor systems, was that these movements were simply an alternating series of reflexes. In the late 1960s and early 1970s, some still shared this belief, whereas others favored Graham Brown’s hypothesis that repetitive movements were centrally programmed and did not depend on reflexes triggered by sensory inputs. There was no strong evidence then for either scenario except for the rhythmic movements of respiration. Lund’s pioneering work during his PhD proved the existence of a central pattern generator (CPG) for mastication in the brainstem. Since then he has been interested in understanding how CPGs function and how sensory feedback works to adjust the motor patterns that they produce. Sections in this tribute article to Lund are written by some of his close collaborators and reflect the evolution of his work throughout the years. The first 4 presentations in this article (by K.-G. Westberg, D. McFarland, A. Kolta, and C. Stohler) highlight various aspects of these interests, and the final 2 presentations (by J. Feine and A. Woda) focus especially on clinical aspects of Lund’s interests. The last section of this article is a final commentary from Professor Lund.

mastication; orofacial movements; pain; trigeminal system

1. Dellow PG, Lund JP. Evidence for central timing of rhythmical mastication. J Physiol (Lond) 1971;215:1–13.

2. Lund JP. Mastication and its control by the brain stem. Crit Rev Oral Biol Med 1991;2:33–64.

3. Nakamura Y, Katakura N. Generation of masticatory rhythm in the brainstem. Neurosci Res 1995;23:1–19.

4. Kolta A, Brocard F, Verdier D, Lund JP. A review of burst generation by trigeminal main sensory neurons. Archs Oral Biol 2007;52:325–328.

5. Olsson KÅ, Westberg K-G. Interneurones in the trigeminal motor system. In: Electromyography of Jaw Reflexes in Man. In: van Steenberghe D, de Laat A (eds). Leuven: Leuven University Press, 1989:19–50.

6. Lund JP, Kolta A. Generation of the central masticatory rhythm and its modification by sensory feedback. Dysphagia 2006;21:167–174.

7. Lund JP, Kolta A, Westberg K-G, Scott G. Brainstem mechanisms underlying feeding behaviors. Curr Opin Neurobiol 1998;8:718–724.

8. Sherrington CS. Reflexes elicitable in the cat from pinna vibrissae and jaws. J Physiol (Lond) 1917;51:404–431.

9. McFarland DH, Smith A, Moore CA, Weber CM. Relationship between amplitude of tremor and reflex responses of the human jaw-closing system. Brain Res 1986;366:272–278.

10. Smith A, Moore CA, Weber CM, McFarland DH, Moon

J. Reflex responses of the human jaw-closing system depend on the locus of intraoral mechanical stimulation. Exper Neurol 1985;90:489–509.

11. Smith A, Moore CA, McFarland DH, Weber CM. Reflex responses of human lip muscles to mechanical stimulation during speech. J Motor Behav 1985;17:148–167.

12. Smith A, McFarland DH, Weber CM, Moore CA. Spatial organization of human perioral reflexes. Experimental Neurol 1986;98:233–248.

13. Smith A, McFarland DH, Weber CM. Interactions between speech and finger movements: An exploration of the dynamic pattern perspective. J Speech Hearing Res 1986;29:471–480.

14. McFarland DH, Lund JP. An investigation of the coupling between respiration, mastication, and swallowing in the awake rabbit. J Neurophysiol 1993;69:95–108.

15. Charbonneau I, Lund JP, McFarland DH. Persistence of respiratory-swallowing coordination after laryngectomy. J Speech Lang Hearing Res 2005;48:34–44.

16. McFarland DH, Lund JP, Gagner M. Effects of posture on the coordination of respiration and swallowing. J Neurophysiol 1994;72:2431–2437.

17. Jobin V, Champagne V, Beauregard J, Charbonneau I, McFarland DH, Kimoff RJ. Swallowing function and upper airway sensation in obstructive sleep apnea. J Appl Physiol 2007;102:1587–1594.

18. Nixon GM, Charbonneau I, Kermack AS, Brouillette RT, McFarland DH. Respiratory-swallowing interactions during sleep in premature infants at term. Respiratory Physiol Neurobiol 2008;160:76–82.

19. McFarland DH. Respiratory markers of conversational interaction. J Speech-Lang Hearing Res 2001;44:128–143.

20. McFarland DH, Tremblay P. Clinical implications of cross-system interactions. Seminars Speech Language 2006;27:300–309.

21. Kolta A, Lund JP, Rossignol S. Modulation of trigeminal mesencephalic spindle afferents during fictive mastication. J Neurophysiol 1990;64:1067–1076.

22. Westberg KG, Kolta A, Clavelou P, Sandstrom G, Lund JP. Evidence for functional compartmentalization of trigeminal muscle spindle afferents during fictive mastication in the rabbit. Eur J Neurosci 2000;12:1145–1154.

23. Verdier D, Lund JP, Kolta A. GABAergic Control of Action potential propagation along axonal branches of mammalian sensory neurons. J Neuroscience 2003;23: 2002–2007.

24. Verdier D, Lund JP, Kolta A. Synaptic inputs to trigeminal primary afferent neurons cause firing and modulate intrinsic oscillatory activity. J Neurophysiol 2004;92: 2444–2455.

25. Westberg K-G, Clavelou P, Sandstrom G, Lund JP. Evidence that trigeminal brainstem interneurons form subpopulations to produce different forms of mastication in the rabbit. J Neurosci 1998;18:6466–6479.

26. Donga R, Lund JP. Discharge patterns of trigeminal commissural last-order interneurons during fictive mastication in the rabbit. J Neurophysiol 1991;66:1564–1578.

27. Tsuboi A, Chen CC, Kolta A, Lund JP. Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci 2003; 17:229–238.

28. Brocard F, Verdier D, Arsenault I, Lund JP, Kolta A. Maturation of persistent sodium current and the emergence of intrinsic burst generation in trigeminal principal sensory nucleus neurons during the acquisition of mastication in weanling rats. J Neurophysiol 2006;96: 2410–2424.

29. Lund JP, Denga R, Widmer CG, Stohler CS. The painadaptation model. Can J Physiol Pharmacol 1991;69: 683–694.

30. Feine JS, Hutchins MO, Lund JP. An evaluation of the criteria used to diagnose mandibular dysfunction with the mandibular kinesiograph. J Prosthet Dent 1988;60: 374–380.

31. Dao TTT, Feine JS, Lund JP. Can electrical stimulation be used to establish a physiologic occlusal position?J Prosthet Dent 1988;60:509–514.

32. Feine JS, Chapman CE, Lund JP, Duncan GH, Bushnell

MC. The perception of painful and non-painful stimuli during voluntary motor activity in man. Somatosen Motor Res 1990;7:113–124.

33. Awad MA, Lund JP, Shapiro SH, et al. Oral health status and treatment satisfaction with mandibular implant overdentures and conventional dentures. A randomized clinical trial in a senior population. Int J Prosthodont 2003;16: 390–396.

34. Lund JP, Lavigne G, Feine JS, et al. The use of electronic devices in the diagnosis and treatment of temporomandibular disorders. J Can Dent Assoc 1989;55: 749–750.

35. Dao TTT, Lavigne GJ, Charbonneau A, Feine JS, Lund JP. The efficacy of oral splints in the treatment of myofascial pain of the jaw muscles: a controlled clinical trial. Pain 1994;56:85–94.

36. Feine JS, Lavigne GJ, Dao TTT, Morin C, Lund JP. Memories of chronic pain and perceptions of relief. Pain 1998;77:137–141.

37. Awad M, Shapiro S, Lund JP, Feine JS. Determinants of patients’ treatment preferences in a clinical trial. Comm Dent Oral Epi 2000;28:119–125. *

38. Morin C, Lund JP, Vilarroel T, Clokie CML, Feine JS. Differences between the sexes in post-surgical pain. Pain 2000;85:79–85.

39. Morais JA, Heydecke G, Pawliuk J, Lund JP, Feine JS. The effect of mandibular two-implant overdentures on nutrition in elderly edentulous individuals. J Dent Res 2003; 82:53–58.

40. Heydecke G, Thomason JM, Lund JP, Feine JS. The impact of conventional and implant supported prostheses on social andsexual activities in edentulous adults. Results from a randomized trial 2 months after treatment. J Dent 2005;33:649–657.

41. Feine JS, Maskawi K, Donohue WB, de Grandmont P, Tanguay R, Lund JP. Within -subject comparisons of implant-supported mandibular prostheses: Evaluation of masticatory function. J Dent Res 1994;73:1646–1656.

42. de Grandmont P, Feine JS, Boudrias P, Taché R, Donohue WB, Tanguay R, Lund JP. Within-subject comparisons of implant-supported mandibular prostheses: Psychometric evaluation. J Dent Res 1994;73:1096–1104.

43. Esfandiari S, Lund J, Thomason M, et al. Can general dentists produce successful implant overdentures with minimal training ? J Dent 2006;34:796–801.

44. Heydecke G, Penrod JR, Takanashi Y, Lund JP, Feine JS, Thomason JM. Cost-effectiveness of mandibular two-implant overdentures and conventional dentures in edentulous seniors. J Dent Res 2005;84:794–799.

45. Lucas PW, Luke DA. Is food particle size a criterion for the initiation of swallowing? J Oral Rehab 1986;13: 127–136.

46. Peyron MA, Mishellany A, Woda A. Particle size distribution of food boluses after mastication of six natural foods. J Dent Res 2004a;83:578–582.

47. Mishellany A, Woda A, Labas R, Peyron MA. The challenge of mastication: Preparing a bolus suitable for deglutition? Dysphagia 2006;21:87–94.

48. Jalabert-Malbos ML, Mishellany-Dutour A, Woda A, Peyron MA. Particle size distribution in the food bolus after mastication of natural foods. Food Quality Preference 2007;18:803–812.

49. Anderson DL. Death from improper mastication. Int Dent J 1977;27:349–354.

50. Prinz JF, Lucas PW. An optimization model for mastication and swallowing in mammals. Proc R Soc Lond B 1997;264:1715–1721.

51. Seo HS, Hwang IK, Han TR, Kim IS. Sensory and instrumental analysis for slipperiness and compliance of food during swallowing. J Food Sci 2007;72:S707–S713.

52. Mishellany A, Renaud J, Peyron MA, Rimek F, Woda A. Is the goal of mastication reached in young dentates, aged dentatesand aged denture wearers? Br J Nutri 2008; 99:121–128.

53. Hiiemae KM, Palmer JB. Food transport and bolus formation during complete feeding sequences on foods of different initial consistency. Dysphagia 1999;14;31–42.

54. Feine JS, Lund JP. Measuring chewing ability in randomized controlled trials with edentulous populations wearing implant prostheses. J Oral Rehabil 2006;33:301–308.

55. Peyron MA, Blanc O, Lund JP, Woda A. Influence of age on adaptability of human mastication. J Neurophysiol 2004b;92:773–779.

56. Feldman RS, Kapur KK, Alman JE, Chauncey HH. Aging and mastication: Changes in performance and in the swallowing threshold with natural dentition. J Am Geriatric Soc 1980;28:97–103.

57. Morais JA, Heydecke G, Pawliuk J, Lund JP, Feine JS. The effects of mandibular two-implant overdentures on nutrition in elderly edentulous individuals. J Dent Res 2003; 82:53–58.

58. Sheiham A, Steele JG, Marcenes W, et al. The relationship among dental status, nutrient intake, and nutritional status in older people. J Dent Res 2001;80:408–413.

59. Faulks D, Hennequin M. Defining the population requiring special care dentistry using the International Classification of Functioning, Disability and Health—A personal view. J Disability Oral Health 2006;7/3; 143–152.

60. Woda A, Foster K, Mishellany A, Peyron MA. Adaptation of healthy mastication to factors pertaining to the individual or to the food. Physiol Behav 2006;89: 28–35.