DOI QR코드

DOI QR Code

RESPONSE CHARACTERISTICS OF VENTRAL POSTEROMEDIAL THALAMIC NOCICEPTIVE NEURONS IN THE ANESTHETIZED RAT

마취된 흰 쥐 시상의 복후내측핵내 유해성 뉴론의 특성

  • Lee, Hyung-Il (Department of Conservative Dentistry, College of Dentistry, Chonbuk National University) ;
  • Park, Soo-Joung (Department of Oral Physiology, College of Dentistry, Chonbuk National University)
  • 이형일 (전북대학교 치과대학 치과보존학교실) ;
  • 박수정 (전북대학교 치과대학 구강생리학교실)
  • Published : 2002.11.01

Abstract

Extracellular single unit recordings were made from the ventral posteromedial thalamic (VPM) nociceptive neurons to determine mechanoreceptive field (RF) and response properties. A total of 44 VPM thalamic nociceptive neurons were isolated from rats anesthetized with urethane-chloralose. Based on responses to various mechanical stimuli including touch, pressure and pinch applied to the RF, 32 of 44 neurons were classified as nociceptive specific (NS) neuron. The other 12 neurons, classified as wide dynamic range (WDR), showed a graded response to increasingly intense stimuli, with a maximum discharge to noxious pinch. The VPM nociceptive neurons showed various spontaneous activity ranged from 0-6 Hz. They were located throughout the VPM, and had an contralateral RF including mainly intraoral (and perioral) regions. The RF size was relatively small, and very few neurons had a receptive field involving 3 trigeminal divisions. The NS neurons activated only by pressure and pinch stimuli had high mechanical thresholds compared to WDR neurons activated also by touch stimuli. The VPM nociceptive neurons were tested with suprathershold graded mechanical stimuli. Most of 21 NS and 8 WDR neurons showed a progressive increase in number of spikes as mechanical stimulus intensity was increased. In some neurons, the responses reached a peak before the highest intensity was given. Application of 5 mM $CoCl_2{\;}(10{\;}{\mu}\ell)$ solution to the trigeminal subnucleus caudalis did not produce any significant changes in the spontaneous activity, RF size, mechanical threshold, and response to suprathreshold mechanical stimuli of 9 VPM nociceptive neurons tested. 17 of 33 VPM nociceptive neurons responded to noxious heat as well as noxious mechanical stimuli applied to their RF. Application of the mustard oil, a small-fiber excitant and inflammatory irritant, to the right maxillary first molar tooth pulp induced an immediate but short-lasting neuronal discharges upto approximately 4 min in 16 of 42 VPM nociceptive neurons. These results suggest that VPM thalamic nucleus may contribute to the sensory discriminative aspect of orofacial nociception.

Keywords

References

  1. Albe-Fsssard, D.. Berkley, K.J.. Kruger, L.. Ralston, H.J. and Willis, W.D. Diencephalic mechanisms of pain sensation. Brain Res. 356: 217-296, 1985
  2. Craig, A.D. and Dostrovsky, J.O. Medulla to Thalamus. In: P.D. Wall and R. Melzack (Eds.), Textbook of Pain, Churchill-Livingstone, Edinburgh, 1999, pp. 183-214
  3. Sessle, B.J. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit. Rev. Oral Biol. Med. 11: 57-91, 2000 https://doi.org/10.1177/10454411000110010401
  4. Apkarian, A.V. and Hodge, C.J. Primate spinothalamic pathways: III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways. J. Comp. Neurol. 288: 493-511, 1989 https://doi.org/10.1002/cne.902880309
  5. Craig, A.D., Linington, A.J. and Kniffki, K.D. Cells of origin of spinothalamic tract projections to the medial and lateral thalamus in the cat. J. Comp. Neurol. 289: 568-585, 1989 https://doi.org/10.1002/cne.902890404
  6. Ganchrow, D. Intratrigeminal and thalamic projections of nucleus caudalis in the squirrel monkey (Saimiri sciureus): a degeneration and autoradiographic study. J. Comp. Neurol. 178: 281-312, 1978 https://doi.org/10.1002/cne.901780206
  7. Casey, K.L. and Morrow T.J. Ventral posterior thalamic neurons differentially responsive to noxious stimulation of the awake monkey. Science. 221: 675-677, 1983 https://doi.org/10.1126/science.6867738
  8. Chung. J.M., Lee, K.H., Surmeier, D.J., Sorkin, L.S., Kim, J. and Willis, W.D. Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J. Neurophysiol. 56: 370-390, 1986 https://doi.org/10.1152/jn.1986.56.2.370
  9. Kenshalo, D.R., Giesler, G.J., Leonard, R.B. and Willis, W.D. Responses of neurons in primate ventral posterior lateral nucleus to noxious stimuli. J. Neurophysiol. 43: 1594-1614, 1980 https://doi.org/10.1152/jn.1980.43.6.1594
  10. Brinkhus, H.B., Carstens, E. and Zimmermann, M. Encoding of graded noxious skin heating by neurons in posterior thalamus and adjacent areas in the cat. Neurosci. Lett. 15: 37-42, 1979 https://doi.org/10.1016/0304-3940(79)91526-X
  11. Honda, C.N., Mense, S. and Perl. E.R. Neurons in ventrobasal region of cat thalamus selectively responsive to noxious mechanical stimulation. J. Neurophysiol. 49: 662-673, 1983 https://doi.org/10.1152/jn.1983.49.3.662
  12. Yokota, T., Asato, F., Koyama, N.. Masuda, T. and Taguchi, H. Nociceptive body representation in nucleus ventralis posterolateralis of cat thalamus. J. Neurophysiol. 60: 1714-1727, 1988 https://doi.org/10.1152/jn.1988.60.5.1714
  13. Simone, D.A., Hanson, M.E., Bernau, N.A. and Pubols, B.H. Nociceptive neurons of the raccoon lateral thalamus. J. Neurophysiol. 69: 318-328, 1993
  14. Benoist, J.M., Kayser, V., Gautron. M. and Guilbaud G. Low dose of morphine strongly depresses responses of specific nociceptive neurones in the ventrobasal complex of the rat. Pain 15: 333-344, 1983 https://doi.org/10.1016/0304-3959(83)90070-2
  15. Guilbaud, G., Peschanski, M., Gautron, M. and Binder, D. Neurones responding to noxious stimulation in VB complex and caudal adjacent regions in the thalamus of the rat. Pain 8: 303-318, 1980 https://doi.org/10.1016/0304-3959(80)90076-7
  16. Mitchell, D. and Hellon, R.F. Neuronal and behavioural responses in rats during noxious stimulation of the tail. Proc. R. Soc, Lond. B BioI. Sci. 197: 169-194, 1977 https://doi.org/10.1126/science.877548
  17. Peschanski, M., Guilbaud, G., Gautron, M. and Besson, J.M. Encoding of noxious heat messages in neurons of the ventrobasal thalamic complex of the rat. Brain Res. 197: 401-413, 1980 https://doi.org/10.1016/0006-8993(80)91125-7
  18. Yokota, T. and Matsumoto, N. Location and functional organization of trigeminal wide dynamic range neurons within the nucleus ventralis posteromedialis of the cat. Neurosci. Lett. 39: 231-236, 1983 https://doi.org/10.1016/0304-3940(83)90305-1
  19. Yokota, T. and Matsumoto, N. Somatotopic distribution of trigeminal nociceptive specific neurons within the caudal somatosensory thalamus of cat. Neurosci. Lett. 39: 125-130, 1983 https://doi.org/10.1016/0304-3940(83)90064-2
  20. Yokota, T., Koyama, N. and Matsumoto, N. Somatotopic distribution of trigeminal nociceptive neurons in ventrobasal complex of cat thalamus. J. Neurophysiol. 53: 1387-1400, 1985 https://doi.org/10.1152/jn.1985.53.6.1387
  21. Bushnell. M.C, and Duncan, G.H. Mechanical response properties of ventroposterior medial thalamic neurons in the alert monkey. Exp. Brain Res. 67: 603-614, 1987
  22. Iwata, K.. Kenshalo D.R.. Dubner, R. and Nahin. R.L. Diencephalic projections from the superficial and deep laminae of the medullary dorsal horn in the rat. J. Comp. Neurol. 321: 404-420, 1992 https://doi.org/10.1002/cne.903210308
  23. Peschanski, M. Trigeminal afferents to the diencephalon in the rat. Neuroscience 12: 465-487, 1984 https://doi.org/10.1016/0306-4522(84)90066-6
  24. Barnett, E.M., Evans, G.D., Sun, N.. Perlman, S. and Cassell, M.D. Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1. J. Neurosci. 15: 2972-84, 1995
  25. Hu, J.W. Response properties of nociceptive and nonnociceptive neurons in the rat's trigeminal subnucleus caudalis (medullary dorsal horn) related to cutaneous and deep craniofacial afferent stimulation and modulation by diffuse noxious inhibitory controls. Pain 41: 331-345,1990 https://doi.org/10.1016/0304-3959(90)90010-B
  26. Vahle-Hinz, C. and Gottschaldt, K.M. Principal differences in the organization of the thalamic face representation in rodents and felids. In: Macchi, G., Rustiont, A. and Spreafico. R. (Eds.), Somatosensory integration in the thalamus, Elsevier Science, Amsterdam, 1983, pp. 125-145
  27. Vos, B.P., Benoist, J.M., Gautron, M. and Guilbaud. G. Changes in neuronal activities in the two ventral posterior medial thalamic nuclei in an experimental model of trigeminal pain in the rat by constriction of one infraorbital nerve. Somatosens. Mot. Res. 17: 109-122, 2000 https://doi.org/10.1080/08990220050020535
  28. Dallel, R., Raboisson, P.. Auroy, P. and Woda, A. The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res. 448: 7-19, 1988 https://doi.org/10.1016/0006-8993(88)91096-7
  29. Shigenaga, Y., Matano, S., Okada, K. and Sakai, A. The effects of tooth pulp stimulation in the thalamus and hypothalamus of the rat. Brain Res. 63: 402-407, 1973 https://doi.org/10.1016/0006-8993(73)90113-3
  30. Yokota, T., Nishikawa, Y. and Koyama, N. Tooth pulp input to the shell region of nucleus ventralis posteromedialis of the cat thalamus. J. Neurophysiol. 56: 80-98, 1986 https://doi.org/10.1152/jn.1986.56.1.80
  31. Allen, G.V. and Pronych, S.P. Trigeminal autonomic pathways involved in nociception-induced reflex cardiovascular responses. Brain Res. 754: 269-278, 1997 https://doi.org/10.1016/S0006-8993(97)00091-7
  32. Hochstenbach, S.L. and Ciriello, J. Medullary pathways mediating depressor responses from Na +-sensitive sites in nucleus of the solitary tract. Am. J. Physiol. 272: R126-133, 1997
  33. Lee, C. and Malpeli. J.G. Somata-selective lesions induced by cobaltous chloride: a parametric study. Brain Res. 364: 396-399, 1986 https://doi.org/10.1016/0006-8993(86)90855-3
  34. Paxinos, G. and Watson, C. The rat brain in stereotaxic coordinates. Academic, New York, 1998. 35
  35. Dallal. R.. Raboisson, P.. Woda, A. and Sessle, B.J. Properties of nociceptive and non-nociceptive neurons in trigeminal subnucleus oralis of the rat. Brain Res. 521: 95-106, 1990 https://doi.org/10.1016/0006-8993(90)91529-P
  36. Park, S.J., Chiang, C.Y.. Hu, J.W. and Sessle, B.J. Neuroplasticity induced by tooth pulp stimulation in trigeminal subnucleus oralis involves NMDA receptor mechanisms. J. Neurophysiol. 85: 1836-1846, 2001 https://doi.org/10.1152/jn.2001.85.5.1836
  37. Cliffer, K.D., Burstein, R. and Giesler, G.J. Distributions of spinothalamic, spinohypothalamic, and spinotelencephalic fibers revealed by anterograde transport of PHA-L in rats. J. Neurosci. 11: 852-868, 1991
  38. Willis, W.D. Nociceptive functions of thalamic neurons. In: Steriade, M., Jones, E.G. and McCormick, D.A. (Eds.), Thalamus, experimental and clinical aspects, Vol. II. Elsevier Science, Amsterdam, 1997, pp. 373-424
  39. Gingold, S.I., Greenspan, J.D. and Apkarian. A.V. Anatomic evidence of nociceptive inputs to primary somatosensory cortex: relationship between spinothalamic terminals and thalamocortical cells in squirrelm monkeys. J. Comp. Neural. 308: 467-490, 1991 https://doi.org/10.1002/cne.903080312
  40. Jones, E.G. and Friedman, D.P. Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. J. Neurophysiol. 48: 521-544, 1982 https://doi.org/10.1152/jn.1982.48.2.521
  41. Bushnell, M.C., Duncan, G.H. and Tremblay, N. Thalamic VPM nucleus in the behaving monkey. I. Multimodal and discriminative properties of thermosensitive neurons. J. Neurophysiol. 69: 739-752, 1993 https://doi.org/10.1152/jn.1993.69.3.739
  42. Friedberg, M.H., Lee, S.M. and Ebner, F.F. Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J. Neurophysiol. 81: 2243-2252, 1999 https://doi.org/10.1152/jn.1999.81.5.2243
  43. Kniffki. K.D. and vahle-Hinz. C. The periphery of the cat's ventroposteromedial nucleus ($VPM_{p}$) : nociceptive neurones. In: Thalamus and Pain, edited by J.M. Besson, G. Guilbaud and M. Peschanski. Amsterdam: Elsevier, 1987, p. 245-257
  44. Emmers, R. Stimulation of the periaqueductal gray subdues sensitized pain in morphine- and meperidinedependent rats. Exp. Neurol. 88: 405-417, 1985
  45. Yoshida, A., Dostrovsky, J.O., Sessle, B.J. and Chiang CY. Trigeminal projections to the nucleus submedius of the thalamus in the rat. J. Comp. Neurol. 307: 609-25, 1991 https://doi.org/10.1002/cne.903070408
  46. Mendell, L.M. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp. Neurol. 16: 316-32, 1966
  47. Woolf, C.J. Windup and central sensitization are not equivalent. Pain. 66: 105-108, 1996 https://doi.org/10.1016/0304-3959(96)03114-4
  48. Li, J., Simone, D.A. and Larson, A.A. Windup leads to characteristics of central sensitization. Pain 79: 75-82, 1999 https://doi.org/10.1016/S0304-3959(98)00154-7
  49. Georgopoulos, A.P. Stimulus-response relations in high-threshold mechanothermal fibers innervating primate glabrous skin. Brain Res. 128: 547-52, 1977 https://doi.org/10.1016/0006-8993(77)90181-0
  50. Gybels, J., Handwerker, H.O. and Van Hees, J. A comparison between the discharges of human nociceptive nerve fibres and the subject's ratings of his sensations. J. Physiol. 292: 193-206, 1979 https://doi.org/10.1113/jphysiol.1979.sp012846
  51. Chiang, C.Y.. Park, S.J.. Kwan, C.L., Hu, J.W. and Sessle, B.J. NMDA receptor mechanisms contribute to neuroplasticity induced in caudalis nociceptive neurons by tooth pulp stimulation. J. Neurophysiol. 80: 2621-2631. 1998
  52. Naftel. J.P., Bernanke, J.M. and Qian, X.-B.: Quantitative study of the apical nerve fibers of adult and juvenile rat molars. Anat. Rec. 238: 507-516, 1994 https://doi.org/10.1002/ar.1092380410
  53. Giesler, G.J., Nahin, R.L. and Madsen, A.M. Postsynaptic dorsal column pathway of the rat. I. Anatomical studies. J. Neurophysiol. 51: 260-275, 1984 https://doi.org/10.1152/jn.1984.51.2.260
  54. Cervero, F., Iggo. A. and Molony, V. Responses of spinocervical tract neurones to noxious stimulation of the skin. J. Physiol. 267: 537-58, 1977 https://doi.org/10.1113/jphysiol.1977.sp011825
  55. Al-Chaer. E.D., Lawand. N.B.. Westlund, K.N. and Willis, W.D. Visceral nociceptive input into the ventral posterolateral nucleus of the thalamus: a new function for the dorsal column pathway. J. Neurophysiol. 76: 2661-2674, 1996 https://doi.org/10.1152/jn.1996.76.4.2661
  56. Fukushima, T. and Kerr, F. W. Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinos a neurons with thalamic connections. J. Comp. Neurol. 183: 169-184, 1979 https://doi.org/10.1002/cne.901830112
  57. Mantle-St. John, L.A. and Tracey, D.J. Somatosensory nuclei in the brainstem of the rat: independent projections to the thalamus and cerebellum. J. Comp. Neurol. 255: 259-271. 1987 https://doi.org/10.1002/cne.902550209
  58. Bruce, L.L., McHaffie, J.G. and Stein, B.E. The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labeling study with fluorescent dyes. J. Comp. Neurol. 262: 315-330, 1987 https://doi.org/10.1002/cne.902620302
  59. Hagiwara, S. and Byerly, L. Calcium channel. Annu. Rev. Neurosci. 4: 69-125, 1981
  60. Marfurt. C.F. and Turner, D.F. The central projections of tooth pulp afferent neurons in the rat as determined by the transganglionic transport of horseradish peroxidase. J. Comp. Neurol. 223: 535-547, 1984 https://doi.org/10.1002/cne.902230406
  61. Broton. J.G. and Rosenfeld, J.P. Effects of trigeminal tractotomy on facial thermal nociception in the rat. Brain Res. 333: 63-72, 1985 https://doi.org/10.1016/0006-8993(85)90124-6
  62. Ikegami, S. and Kawamura, H. Avoidance conditioning to tooth pulp stimulation in the cat after bulbar transection. Physiol, Behav. 23: 593-596, 1979 https://doi.org/10.1016/0031-9384(79)90062-3
  63. Young, R.F. Effect of trigeminal tractotomy on dental sensation in humans. J. Neurosurg. 56: 812-818, 1982 https://doi.org/10.3171/jns.1982.56.6.0812
  64. Young, R.F .. Oleson, T.D. and Perryman, K.M. Effect of trigeminal tractotomy on behavioral response to dental pulp stimulation in the monkey. J. Nourosurg. 55: 420-423, 1981 https://doi.org/10.3171/jns.1981.55.3.0420