Warning: mkdir(): Permission denied in /home/virtual/lib/view_data.php on line 81

Warning: fopen(upload/ip_log/ip_log_2024-12.txt): failed to open stream: No such file or directory in /home/virtual/lib/view_data.php on line 83

Warning: fwrite() expects parameter 1 to be resource, boolean given in /home/virtual/lib/view_data.php on line 84
Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat


Your browser does not support the NLM PubReader view.

Go to this page to see a list of supporting browsers.

Response characteristics of ventral posteromedial thalamic nociceptive neurons in the anesthetized rat

Article information

Restor Dent Endod. 2002;27(6):587-599
Publication date (electronic) : 2002 November 30
doi : https://doi.org/10.5395/JKACD.2002.27.6.587
Hyung-Il Lee, Soo-Joung Park*
Department of Conservative Dentistry, College of Dentistry, Chonbuk National University, Korea.
*Department of Oral Physiology and Institute of Oral Bioscience, College of Dentistry, Chonbuk National University, Korea.

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 CoCl2 (10 µl) solution to the trigeminal subnucleus caudalis did not produce any significant changes in the spontaneous activity, RF size, mechanical threshold, and response to suprathresold 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: VPM; orofacial nociception; rat

References

1. Albe-Fessard D, Berkley KJ, Kruger L, Ralston HJ, Willis WD. Diencephalic mechanisms of pain sensation. Brain Res 1985. 356217–296.
2. Craig AD, Dostrovsky JO. In : Wall PD, Melzack R, eds. Medulla to Thalamus. Textbook of Pain 1999. Edinburgh: Churchill-Livingstone; 183–214.
3. Sessle BJ. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000. 1157–91.
4. Apkarian AV, Hodge CJ. Primate spinothalamic pathways: III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways. J Comp Neurol 1989. 288493–511.
5. Craig AD, Linington AJ, Kniffki KD. Cells of origin of spinothalamic tract projections to the medial and lateral thalamus in the cat. J Comp Neurol 1989. 289568–585.
6. Ganchrow D. Intratrigeminal and thalamic projections of nucleus caudalis in the squirrel monkey (Saimiri sciureus): a degeneration and autoradiographic study. J Comp Neurol 1978. 178281–312.
7. Casey KL, Morrow TJ. Ventral posterior thalamic neurons differentially responsive to noxious stimulation of the awake monkey. Science 1983. 221675–677.
8. Chung JM, Lee KH, Surmeier DJ, Sorkin LS, Kim J, Willis WD. Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J Neurophysiol 1986. 56370–390.
9. Kenshalo DR, Giesler GJ, Leonard RB, Willis WD. Responses of neurons in primate ventral posterior lateral nucleus to noxious stimuli. J Neurophysiol 1980. 431594–1614.
10. Brinkhus HB, Carstens E, Zimmermann M. Encoding of graded noxious skin heating by neurons in posterior thalamus and adjacent areas in the cat. Neurosci Lett 1979. 1537–42.
11. Honda CN, Mense S, Perl ER. Neurons in ventrobasal region of cat thalamus selectively responsive to noxious mechanical stimulation. J Neurophysiol 1983. 49662–673.
12. Yokota T, Asato F, Koyama N, Masuda T, Taguchi H. Nociceptive body representation in nucleus ventralis posterolateralis of cat thalamus. J Neurophysiol 1988. 601714–1727.
13. Simone DA, Hanson ME, Bernau NA, Pubols BH. Nociceptive neurons of the raccoon lateral thalamus. J Neurophysiol 1993. 69318–328.
14. Benoist JM, Kayser V, Gautron M, Guilbaud G. Low dose of morphine strongly depresses responses of specific nociceptive neurones in the ventrobasal complex of the rat. Pain 1983. 15333–344.
15. Guilbaud G, Peschanski M, Gautron M, Binder D. Neurones responding to noxious stimulation in VB complex and caudal adjacent regions in the thalamus of the rat. Pain 1980. 8303–318.
16. Mitchell D, Hellon RF. Neuronal and behavioural responses in rats during noxious stimulation of the tail. Proc R Soc Lond B Biol Sci 1977. 197169–194.
17. Peschanski M, Guilbaud G, Gautron M, Besson JM. Encoding of noxious heat messages in neurons of the ventrobasal thalamic complex of the rat. Brain Res 1980. 197401–413.
18. Yokota T, Matsumoto N. Location and functional organization of trigeminal wide dynamic range neurons within the nucleus ventralis posteromedialis of the cat. Neurosci Lett 1983. 39231–236.
19. Yokota T, Matsumoto N. Somatotopic distribution of trigeminal nociceptive specific neurons within the caudal somatosensory thalamus of cat. Neurosci Lett 1983. 39125–130.
20. Yokota T, Koyama N, Matsumoto N. Somatotopic distribution of trigeminal nociceptive neurons in ventrobasal complex of cat thalamus. J Neurophysiol 1985. 531387–1400.
21. Bushnell MC, Duncan GH. Mechanical response properties of ventroposterior medial thalamic neurons in the alert monkey. Exp Brain Res 1987. 67603–614.
22. Iwata K, Kenshalo DR, Dubner R, Nahin RL. Diencephalic projections from the superficial and deep laminae of the medullary dorsal horn in the rat. J Comp Neurol 1992. 321404–420.
23. Peschanski M. Trigeminal afferents to the diencephalon in the rat. Neuroscience 1984. 12465–487.
24. Barnett EM, Evans GD, Sun N, Perlman S, Cassell MD. Anterograde tracing of trigeminal afferent pathways from the murine tooth pulp to cortex using herpes simplex virus type 1. J Neurosci 1995. 152972–2984.
25. Hu JW. 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 1990. 41331–345.
26. Vahle-Hinz C, Gottschaldt KM. Macchi G, Rustiont A, Spreafico R. Principal differences in the organization of the thalamic face representation in rodents and felids. Somatosensory integration in the thalamus 1983. Amsterdam: Elsevier Science; 125–145.
27. Vos BP, Benoist JM, Gautron M, 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 2000. 17109–122.
28. Dallel R, Raboisson P, Auroy P, Woda A. The rostral part of the trigeminal sensory complex is involved in orofacial nociception. Brain Res 1988. 4487–19.
29. Shigenaga Y, Matano S, Okada K, Sakai A. The effects of tooth pulp stimulation in the thalamus and hypothalamus of the rat. Brain Res 1973. 63402–407.
30. Yokota T, Nishikawa Y, Koyama N. Tooth pulp input to the shell region of nucleus ventralis posteromedialis of the cat thalamus. J Neurophysiol 1986. 5680–98.
31. Allen GV, Pronych SP. Trigeminal autonomic pathways involved in nociception-induced reflex cardiovascular responses. Brain Res 1997. 754269–278.
32. Hochstenbach SL, Ciriello J. Medullary pathways mediating depressor responses from Na+-sensitive sites in nucleus of the solitary tract. Am J Physiol 1997. 272R126–R133.
33. Lee C, Malpeli JG. Somata-selective lesions induced by cobaltous chloride: a parametric study. Brain Res 1986. 364396–399.
34. Paxinos G, Watson C. The rat brain in stereotaxic coordinates 1998. New York: Academic;
35. Dallel R, Raboisson P, Woda A, Sessle BJ. Properties of nociceptive and non-nociceptive neurons in trigeminal subnucleus oralis of the rat. Brain Res 1990. 52195–106.
36. Park SJ, Chiang CY, Hu JW, Sessle BJ. Neuroplasticity induced by tooth pulp stimulation in trigeminal subnucleus oralis involves NMDA receptor mechanisms. J Neurophysiol 2001. 851836–1846.
37. Cliffer KD, Burstein R, Giesler GJ. Distributions of spinothalamic, spinohypothalamic, and spinotelencephalic fibers revealed by anterograde transport of PHA-L in rats. J Neurosci 1991. 11852–868.
38. Willis WD. In : Steriade M, Jones EG, McCormick DA, eds. Nociceptive functions of thalamic neurons. Thalamus, experimental and clinical aspects, Vol. II 1997. Amsterdam: Elsevier Science; 373–424.
39. Gingold SI, Greenspan JD, Apkarian AV. Anatomic evidence of nociceptive inputs to primary somatosensory cortex: relationship between spinothalamic terminals and thalamocortical cells in squirrel monkeys. J Comp Neurol 1991. 308467–490.
40. Jones EG, Friedman DP. Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. J Neurophysiol 1982. 48521–544.
41. Bushnell MC, Duncan GH, Tremblay N. Thalamic VPM nucleus in the behaving monkey I Multimodal and discriminative properties of thermosensitive neurons. J Neurophysiol 1993. 69739–752.
42. Friedberg MH, Lee SM, Ebner FF. Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol 1999. 812243–2252.
43. Kniffki KD, vahle-Hinz C. Besson JM, Guilbaud G, Peschanski M. The periphery of the cat's ventroposteromedial nucleus (VPMp): nociceptive neurones. Thalamus and Pain 1987. Amsterdam: Elsevier; 245–257.
44. Emmers R. Stimulation of the periaqueductal gray subdues sensitized pain in morphine- and meperidinedependent rats. Exp Neurol 1985. 88405–417.
45. Yoshida A, Dostrovsky JO, Sessle BJ, Chiang CY. Trigeminal projections to the nucleus submedius of the thalamus in the rat. J Comp Neurol 1991. 307609–625.
46. Mendell LM. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 1966. 16316–332.
47. Woolf CJ. Windup and central sensitization are not equivalent. Pain 1996. 66105–108.
48. Li J, Simone DA, Larson AA. Windup leads to characteristics of central sensitization. Pain 1999. 7975–82.
49. Georgopoulos AP. Stimulus-response relations in high-threshold mechanothermal fibers innervating primate glabrous skin. Brain Res 1977. 128547–552.
50. Gybels J, Handwerker HO, Van Hees J. A comparison between the discharges of human nociceptive nerve fibres and the subject's ratings of his sensations. J Physiol 1979. 292193–206.
51. Chiang CY, Park SJ, Kwan CL, Hu JW, Sessle BJ. NMDA receptor mechanisms contribute to neuroplasticity induced in caudalis nociceptive neurons by tooth pulp stimulation. J Neurophysiol 1998. 802621–2631.
52. Naftel JP, Bernanke JM, Qian XB. Quantitative study of the apical nerve fibers of adult and juvenile rat molars. Anat Rec 1994. 238507–516.
53. Giesler GJ, Nahin RL, Madsen AM. Postsynaptic dorsal column pathway of the rat. I. Anatomical studies. J Neurophysiol 1984. 51260–275.
54. Cervero F, Iggo A, Molony V. Responses of spinocervical tract neurones to noxious stimulation of the skin. J Physiol 1977. 267537–558.
55. Al-Chaer ED, Lawand NB, Westlund KN, Willis WD. Visceral nociceptive input into the ventral posterolateral nucleus of the thalamus: a new function for the dorsal column pathway. J Neurophysiol 1996. 762661–2674.
56. Fukushima T, Kerr FW. Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections. J Comp Neurol 1979. 183169–184.
57. Mantle-St John LA, Tracey DJ. Somatosensory nuclei in the brainstem of the rat: independent projections to the thalamus and cerebellum. J Comp Neurol 1987. 255259–271.
58. Bruce LL, McHaffie JG, Stein BE. The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labeling study with fluorescent dyes. J Comp Neurol 1987. 262315–330.
59. Hagiwara S, Byerly L. Calcium channel. Annu Rev Neurosci 1981. 469–125.
60. Marfurt CF, Turner DF. The central projections of tooth pulp afferent neurons in the rat as determined by the transganglionic transport of horseradish peroxidase. J Comp Neurol 1984. 223535–547.
61. Broton JG, Rosenfeld JP. Effects of trigeminal tractotomy on facial thermal nociception in the rat. Brain Res 1985. 33363–72.
62. Ikegami S, Kawamura H. Avoidance conditioning to tooth pulp stimulation in the cat after bulbar transection. Physiol Behav 1979. 23593–596.
63. Young RF. Effect of trigeminal tractotomy on dental sensation in humans. J Neurosurg 1982. 56812–818.
64. Young RF, Oleson TD, Perryman KM. Effect of trigeminal tractotomy on behavioral response to dental pulp stimulation in the monkey. J Neurosurg 1981. 55420–423.

Article information Continued

Copyright © 2002 Korean Academy of Conservative Dentistry
(open-access) :

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Fig. 1

Fig. 1

Location of the histologically confirmed recording sites plotted on the diagram of ventral posteromedial thalamic (VPM) nucleus. Coronal section of rat brain at 3.3 mm posterior to the Bregma (Paxinos and Watson, 1998). Filled circles show the location of nociceptive specific neurons, whereas open circles show the location of wide dynamic range neurons. VPM, ventral posteromedial thalamic nucleus; VPL, ventral posterolateral thalamic nucleus; PO, posterior thalamic nuclei; ic, internal capsule; mt, mammillothalamic tract; f, fornix.

Fig. 2

Fig. 2

Example of receptive field (RF) and response properties of VPM nociceptive neuron. A: nociceptive specific neuron, B: wide dynamic range neuron. RF: The dot represents the spot from which the neuron could be activated. Threshold: Line over the action potentials showing the mechanical force applied to the RF. Pinch response: The stimulus-response curve (force vs firing rate) of neuron. RH: Peristimulus time histogram (PSTH) showing the response to radiant heat applied to the RF. The bar indicates the duration (3 sec) of the stimulus. MO: PSTH showing the response to mustard oil (MO) applied into the right maxillary first molar pulp. The arrow indicates the time of MO application.

Fig. 3

Fig. 3

Histogram showing percentage of ventral posteromedial thalamic (VPM), trigeminal subnucleus caudalis (Vc) and oralis (Vo) nociceptive neurons having a mechanoreceptive field limited within one V division (1 DIV) or involving two (2 DIV) or all three trigeminal divisions (3 DIV), and a mechanoreceptive field involving intraoral (IO) region. A: NS neuron, B: WDR neuron. Vc data reported by Hu, J.W., Pain, 1990. Vo data reported by Park et al., J. Neurophysiol. 2001.

Fig. 4

Fig. 4

The dot raster display showing response of a VPM WDR neuron to repetitive (1 Hz, 1 mA, 0.2 ms or 2 ms) electrical stimulation of its receptive field. A single dot represents the occurrence of a single action potential; rows represent successive responses shown from top (first stimulus) to bottom (20th stimulus). Note the "wind-up" of the neuron's C fiber evoked responses to successive electrical stimuli in lower trace.

Fig. 5

Fig. 5

Distribution of mechanical threshold of individual VPM nociceptive neurons. A: NS neuron (n=32), B: WDR neuron (n=12). Inset shows mean mechanical threshold ± S.E.

Fig. 6

Fig. 6

Stimulus-response curve of individual VPM nociceptive neuron to graded mechanical stimuli. A: NS neuron (n=21), B: WDR neuron (n=8). Mean stimulus-response curve is drawn with the thick line. Note that WDR and NS neurons showed a progressive increase in number of spikes as mechanical stimulus intensity was increased.

Table 2

Changes in RF and neuronal response properties of VPM nociceptive neurons following application of CoCl2 or saline to trigeminal subnucleus caudalis in adult rats

Table 2

All values are shown as mean ± S.E. Note that RF and neuronal response properties are not significantly changed after CoCl2 or saline application (Wilcoxon signed rank test).