The functional anatomy of lamina I and its role in post-stroke central pain

Progress in Brain Research

Volumn 129, Issue , 2000, Pages 137-151

  Craig, A D ^a  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; ARTICLE; HEAT SENSITIVITY; HUMAN; HYPOTHALAMUS; NERVE CELL; NERVE FIBER C; NEUROANATOMY; NOCICEPTION; PAIN; PARABRACHIAL NUCLEUS; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; SENSORY NERVE; SPINAL CORD DORSAL HORN; SPINOTHALAMIC TRACT; STROKE;

EID: 0034589407     PISSN: 00796123     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0079-6123(00)29010-9     Document Type: Article

References (119)

1. Adelson, D.W., Wei, J.Y. and Kruger, L. (1997) Warm-sensitive afferent splanchnic C-fiber units in vitro. J. Neurophysiol., 77: 2989-3002.
2. Allen, G.V., Saper, C.B., Hurley, K.M. and Cechetto, D.F. (1991) Organization of visceral and limbic connections in the insular cortex of the rat. J. Comp. Neurol., 311: 1-16.
3. Andrew, D. and Craig, A.D. (1999a) Histamine-selective lamina I spinothalamic tract neurons. Soc. Neurosci. Abstr., 25: 149.
4. Andrew, D. and Craig, A.D. (1999b) Responses of lamina I spinothalamic tract (STT) cells to tonic noxious mechanical stimuli. IASP World Congress on Pain.
5. Andrew, D. and Greenspan, J.D. (1999) Peripheral coding of tonic mechanical cutaneous pain: Comparison of nociceptor activity in rat and human psychophysics. J. Neurophysiol., 82: 2641-2648.
6. Apkarian, A.V., Stea, R.A. and Bolanowski, S.J. (1994) Heat-induced pain diminishes vibrotactile perception: A touch gate. Somatosens. Mot. Res., 11: 259-267.
7. Beric, A. (1997) Post-spinal cord injury pain states (editorial). Pain, 72: 295-298.
8. Berthier, M.L., Starkstein, S.E. and Leiguarda, R.C. (1988) Asymbolia for pain: A sensory-limbic disconnection syndrome. Ann. Neurol., 24: 41-49.
9. Beydoun, A., Morrow, T.J. and Casey, K.L. (1997) Pain-related laser-evoked potentials in awake monkeys: Identification of components, behavioral correlates and drug effects. Pain, 72: 319-324.
10. Bini, G., Cruccu, G., Hagbarth, K.-E., Schady, W. and Torebjörk, E. (1984) Analgesic effect of vibration and cooling on pain induced by intraneural electrical stimulation. Pain, 18: 239-248.
11. Blatteis, C.M. (Ed.) (1998) Physiology and Pathophysiology of Temperature Regulation. World Scientific, Singapore.
12. Blomqvist, A., Zhang, E.-T. and Craig, A.D. (2000) Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the VMpo nucleus, in the human thalamus. Brain, 123: 601-619.
13. Boivie, J. and Leijon, G. (1991) Clinical findings in patients with central poststroke pain. In: K.L. Casey (Ed.), Pain and Central Nervous System Disease: The Central Pain Syndromes. Raven Press, New York, pp. 65-76.
14. Bowsher, D. (1996) Central pain: Clinical and physiological characteristics. J. Neurol. Neurosurg. Psychiatry, 61: 62-69.
15. Bowsher, D., Leijon, G. and Thoumas, K.A. (1998) Central poststroke pain - Correlation of MRI with clinical pain characteristics and sensory abnormalities. Neurology, 51: 1352-1358.
16. Bromm, B., Scharein, E. and Vahle-Hinz, C. (2000) Cortex areas involved in the processing of normal and altered pain. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129, Elsevier, Amsterdam, pp. 289-302.
17. Bushnell, M.C. and Duncan, G.H. (1989) Sensory and affective aspects of pain perception: Is medial thalamus restricted to emotional issues. Exp. Brain Res., 78: 415-418.
18. Bushnell, M.C., Duncan, G.H., Dubner, R. and He, L.F. (1984) Activity of trigeminothalamic neurons in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. J. Neurophysiol., 52: 170-187.
19. Calford, M.B. and Tweedale, R. (1991) C-fibres provide a source of masking inhibition to primary somatosensory cortex. Proc. R. Soc. Lond. B, 243: 269-275.
20. Campero, M., Serra, J. and Ochoa, J.L. (1996) C-polymodal nociceptors activated by noxious low temperature in human skin. J. Physiol. (Paris), 497: 565-572.
21. Casey, K.L. (2000) Concepts of pain mechanisms: The contribution of functional imaging of the human brain. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129, Elsevier, Amsterdam, pp. 277-287.
22. Cesaro, P., Mann, M.W., Moretti, J.L., Defer, G., Roualdès, B., Nguyen, J.P. and Degos, J.D. (1991) Central pain and thalamic hyperactivity: A single photon emission computerized tomographic study. Pain, 47: 329-336.
23. Crabtree, J.W., Collingridge, G.L. and Isaac, J.T. (1998) A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus (see comments). Nat. Neurosci., 1: 389-394.
24. Craig, A.D. (1993) Propriospinal input to thoracolumbar sympathetic nuclei from cervical and lumbar lamina I neurons in the cat and the monkey. J. Comp. Neurol., 331: 517-530.
25. Craig, A.D. (1995a) Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J. Comp. Neurol., 361: 225-248.
26. Craig, A.D. (1995b) Supraspinal projections of lamina I neurons. In: J.-M. Besson and G.O.H. Guilbaud (Eds.), Forebrain Areas Involved in Pain Processing. Libbey, Paris, pp. 13-26.
27. Craig, A.D. (1996a) Pain, temperature, and the sense of the body. In: O. Franzen, R. Johansson and L. Terenius (Eds.), Somesthesis and the Neurobiology of the Somatosensory Cortex. Birkhäuser, Basle, pp. 27-39.
28. Craig, A.D. (1996b) An ascending general homeostatic afferent pathway originating in lamina I. In: G. Holstege, R. Bandler and C.B. Saper (Eds.), The Emotional Motor System, Elsevier, Amsterdam, pp. 225-242.
29. Craig, A.D. (1997) The primate MDvc contains nociceptive neurons. Soc. Neurosci. Abstr., 23: 1012.
30. Craig, A.D. (1998) A new version of the thalamic disinhibition hypothesis of central pain. Pain Forum, 7: 1-14.
31. Craig, A.D. (2000) Spinal location of ascending lamina I axons in the macaque monkey. J. Pain, 1: 33-45.
32. Craig, A.D. and Andrew, D. (1999) Lamina I spinothalamic neurons display temporal summation to repeated brief contact heat stimuli. Soc. Neurosci. Abstr., 25: 148.
33. Craig, A.D. and Bushnell, M.C. (1994) The thermal grill illusion: Unmasking the burn of cold pain. Science, 265: 252-255.
34. Craig, A.D. and Dostrovsky, J.O. (1999) Medulla to thalamus. In: P.D. Wall and R. Melzack (Eds.), Textbook of Pain. Lea and Fibiger, Philadelphia, PA, pp. 183-214.
35. Craig, A.D. and Kniffki, K.-D. (1985) Spinothalamic lumbosacral lamina I cells responsive to skin and muscle stimulation in the cat. J. Physiol., 365: 197-221.
36. Craig, A.D. and Serrano, L.P. (1994) Effects of systemic morphine on lamina I spinothalamic tract neurons in the cat. Brain Res., 636: 233-244.
37. Craig, A.D. and Zhang, E.-T. (1996) Anterior cingulate projection from MDvc (a lamina I spinothalamic target in the medial thalamus of the monkey), Soc. Neurosci. Abstr. 22.
38. Craig, A.D., Bushnell, M.C., Zhang, E.-T. and Blomqvist, A. (1994) A thalamic nucleus specific for pain and temperature sensation. Nature, 372: 770-773.
39. Craig, A.D., Reiman, E.M., Evans A. and Bushnell, M.C. (1996) Fuctional imaging of an illusion of pain. Nature, 384: 258-260.
40. Craig, A.D., Zhang, E.-T. and Blomqvist, A. (1998) Immunohistochemical identification of ascending lamina I axons in the lateral spinothalamic tract. Soc. Neurosci. Abstr., 24: 387.
41. Craig, A.D., Zhang, E.T. and Blomqvist, A. (1999) A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey. J. Comp. Neurol., 404: 221-234.
42. Craig, A.D., Chen, K., Bandy, D. and Reiman, E.M. (2000) Thermosensory activation of insular cortex. Nat. Neurosci., 3: 184-190.
43. Davies, S.N., Goldsmith, G.E., Hellon, R.F. and Mitchell, D. (1983) Facial sensitivity to rates of temperature change: Neurophysiological and psychophysical evidence from cats and humans. J. Physiol., 344: 161-175.
44. Davis, K.D., Hutchison, W.D., Lozano, A.M. and Dostrovsky, J.O. (1994) Altered pain and temperature perception following cingulotomy and capsulotomy in a patient with schizoaffective disorder. Pain, 59: 189-199.
45. Davis, K.D., Kiss, Z.H.T., Tasker, R.R. and Dostrovsky, J.O. (1996) Thalamic stimulation-evoked sensations in chronic pain patients and in nonpain (movement disorder) patients. J. Neurophysiol., 75: 1026-1037.
46. Davis, K.D., Kwan, C.L., Crawley, A.P. and Mikulis, D.J. (1998a) Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. J. Neurophysiol., 80: 1533-1546.
47. Davis, K.D., Kiss, Z.H.T., Luo, L., Tasker, R.R., Lozano, A.M. and Dostrovsky, J.O. (1998b) Phantom sensations generated by thalamic microstimulation. Nature, 391: 385-387.
48. Davis, K.D., Lozano, A.M., Manduch, M., Tasker, R.R., Kiss, Z.H.T. and Dostrovsky, J.O. (1999) Thalamic relay site for cold perception in humans. J. Neurophysiol., 81: 1970-1973.
49. De Felipe, C., Herrero, J.F., O'Brien, J.A., Palmer, J.A., Doyle, C.A., Smith, A.J.H., Laird, J.M.A., Belmonte, C., Cervero, F. and Hunt, S.P. (1998) Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature, 392: 394-397.
50. Derbyshire, S.W.G. and Jones, A.K.P. (1998) Cerebral responses to a continual tonic pain stimulus measured using positron emission tomography. Pain, 76: 127-135.
51. Di Piero, V., Jones, A.K.P., Iannotti, F., Powell, M., Perani, D., Lenzi, G.L. and Frackowiak, R.S.J. (1991) Chronic pain: A PET study of the central effects of percutaneous high cervical cordotomy. Pain, 46: 9-12.
52. Dostrovsky, J.O. (2000) Role of thalamus in pain. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129, Elsevier, Amsterdam, pp. 245-257.
53. Dostrovsky, J.O. and Craig, A.D. (1996a) Cooling-specific spinothalamic neurons in the monkey. J. Neurophysiol., 76: 3656-3665.
54. Dostrovsky, J.O. and Craig, A.D. (1996b) Nociceptive neurons in primate insular cortex. Soc. Neurosci. Abstr., 22: 111.
55. Duncan, G.H., Kupers, R.C., Marchand, S., Villemure, J.G., Gybels, J.M. and Bushnell, M.C. (1998) Stimulation of human thalamus for pain relief: Possible modulatory circuits revealed by positron emission tomography. J. Neurophysiol., 80: 3326-3330.
56. Foltz, E.L. and White, L.E.J. (1962) Pain relief by frontal cingulotomy. J. Neurosurgery, 19: 89-100.
57. Fruhstorfer, H. and Lindblom, V. (1983) Vascular participation in deep cold pain. Pain, 17: 235-242.
58. Georgopoulos, A.P. (1976) Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin. J. Neurophysiol., 39: 71-83.
59. Greenspan, J.D. and Winfield, J.A. (1992) Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum. Pain, 50: 29-39.
60. Gybels, J.M. and Sweet, W.H. (1989) Neurosurgical Treatment of Persistent Pain. Physiological and Pathological Mechanisms of Human Pain, Karger, Basle.
61. Han, Z.-S., Zhang, E.-T. and Craig, A.D. (1998) Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nat. Neurosci., 1: 218-225.
62. Head, H. and Holmes, G. (1911) Sensory disturbances from cerebral lesions. Brain, 34: 102-254.
63. Hensel, H. (1981) Thermoreception and Temperature Regulation. Academic Press, London.
64. Holstege, G. (1988) Direct and indirect pathways to lamina I in the medulla oblongata and spinal cord of the cat. In: H.L. Fields and J.M. Besson. (Eds.), Progress in Brain Research, Vol. 77. Elsevier, Amsterdam, pp. 47-94.
65. Hsieh, J.-C., Hägermark, O., Ståhle-Bäckdahl, M., Ericson, K., Eriksson, L., Stone-Elander, S. and Ingvar, M. (1994) Urge to scratch represented in the human cerebral cortex during itch. J. Neurophysiol. 72: 3004-3008.
66. Hsieh, J.C., Belfrage, M., Stone-Elander, S., Hansson, P. and Ingvar, M. (1995) Central representation of chronic ongoing neuropathic pain studied by positron emission tomography. Pain, 63: 225-236.
67. Hutchison, W.D., Davis, K.D., Lozano, A.M., Tasker, R.R. and Dostrovsky, J.O. (1999) Pain-related neurons in the human cingulate cortex. Nat. Neurosci., 2: 403-405.
68. Hylden, J.L.K., Nahin, R.L., Traub, R.J. and Dubner, R. (1989) Expansion of receptive fields of spinal lamina I projection neurons in rats with unilateral adjuvant-induced inflammation: The contribution of dorsal horn mechanisms. Pain, 37: 229-243.
69. Iadarola, M.J., Max, M.B., Berman, K.F., Byas-Smith, M.G., Coghill, R.C., Gracely, R.H. and Bennett, G.J. (1995) Unilateral decrease in thalamic activity observed with positron emission tomography in patients with chronic neuropathic pain. Pain, 63: 55-64.
70. Jeanmonod, D., Magnin, M. and Morel, A. (1994) A thalamic concept of neurogenic pain. Proc. 7th Cong. Pain, 2: 767-787.
71. Jeanmonod, D., Magnin, M. and Morel, A. (1998) Chronic neurogenic pain and the medial thalamotomy. Schweiz. Rundschau Med., 83(23): 702-707.
72. Kendall, D. (1939) Some observations on central pain. Brain, 62: 253-273.
73. Kress, M., Koltzenburg, M., Reeh, P.W. and Handwerker, H.O. (1992) Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J. Neurophysiol., 68: 581-595.
74. Krout, K.E., Jansen, A.S.P. and Loewy, A.D. (1998) Periaqueductal gray matter projection to the parabrachial nucleus in rat. J. Comp. Neurol., 401: 437-454.
75. LaMotte, R.H. and Thalhammer, J.G. (1982) Response properties of high-threshold cutaneous cold receptors in the primate. Brain Res., 244: 279-287.
76. Lenz, F.A. and Dougherty, P.M. (1997) Pain processing in the human thalamus. In: M. Steriade, E.G. Jones and D.A. Mc-Cormick (Eds.), Thalamus, Vol. II, Experimental and Clinical Aspects. Elsevier, Amsterdam, pp. 617-652.
77. Lenz, F.A., Lee, J.-I., Garonzik, I.-M., Rowland L.H., Dougherty, P.M. and Hua, S.E. (2000) Human thalamus reorganization related to nervous system injury and dystonia. In: J. Sandkühler, B. Bromm and G.F. Gebhart (Eds.), Nervous System Plasticity and Chronic Pain, Progress in Brain Research, Vol. 129, Elsevier, Amsterdam, pp. 259-273.
78. Logothetis, N.K., Guggenberger, H., Peled, S. and Pauls, J. (1999) Functional imaging of the monkey brain. Nat. Neurosci., 2: 555-562.
79. Lorenz, J., Kohlhoff, H., Hansen, H.C., Kunze, K. and Bromm, B. (1998) Ab-fiber mediated activation of cingulate cortex as correlate of central post-stroke pain. NeuroReport, 9: 659-663.
80. Mantyh, P.W., Rogers, S.D., Honore, P., Allen, B.J., Ghilardi, J.R., Li, J., Daughters, R.S., Lappi, D.A., Wiley, R.G. and Simone, D.A. (1997) Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science, 278: 275-279.
81. Mehler, W.R. (1966) The posterior thalamic region in man. Confin. Neurol., 27: 18-29.
82. Mesulam, M.-M. and Mufson, E.J. (1982) Insula of the old world monkey. III: Efferent cortical output and comments on function. J. Comp. Neurol., 212: 38-52.
83. Morgan, C.W., Ohara, P.T. and Scott, D.E. (1999) Vasoactive intestinal polypeptide in sacral primary sensory pathways in the cat. J. Comp. Neurol., 407: 381-394.
84. Mower, G. (1976) Perceived intensity of peripheral thermal stimuli is independent of internal body temperature. J. Comp. Physiol. Psychol., 90: 1152-1155.
85. Nathan, P.W. and Smith, M.C. (1979) Clinico-anatomical correlation in anterolateral cordotomy. In: J.J. Bonica (Ed.), Advances in Pain Research and Therapy, Vol. 3. Raven Press, New York, pp. 921-926.
86. Norrsell, U. and Craig, A.D. (1999) Behavioral thermosensitivity after lesions of thalamic target areas of a thermosensory spinothalamic pathway in the cat. J. Neurophysiol., 82: 611- 625.
87. Pagni, C.A. and Canavero, S. (1995) Functional thalamic depression in a case of reversible central pain due to a spinal intramedullary cyst. Case report. J. Neurosurg., 83: 163-165.
88. Pan, B., Castro-Lopes, J.M. and Coimbra, A. (1998) Central afferent projection conveying nociceptive input to the PVN as revealed by a combination of anterograde and retrograde labelling with c-fos activation by pain. Soc. Neurosci. Abstr., 24: 1378.
89. Perl, E.R. (1984) Pain and nociception. In: I. Darian-Smith (Ed.), Handbook of Physiology, Section 1, The Nervous System, Vol. III, Sensory Processes, American Physiological Society, Bethesda, MD, pp. 915-975.
90. Perl, E.R. (1996) Pain and the discovery of nociceptors. In: C. Belmonte and F. Cervero (Eds.), Neurobiology of Nociceptors, Oxford University Press, Oxford, pp. 5-36.
91. Peyron, R., García-Larrea, L., Grégoire, M.C., Convers, P., Lavenne, F., Veyre, L., Froment, J.C., Mauguière, F., Michel, D. and Laurent, B. (1998) Allodynia after lateral-medullary (Wallenberg) infarct - A PET study. Brain, 121: 345-356.
92. Pritchard, T.C., Hamilton, R.B., Morse, J.R. and Norgren, R. (1986) Projections of thalamic gustatory and lingual areas in the monkey Macaca fascicularis. J. Comp. Neurol., 244: 213-228.
93. Radhakrishnan, V., Tsoukatos, J., Davis, K.D., Tasker, R.R., Lozano, A.M. and Dostrovsky, J.O. (1999) A comparison of the burst activity of lateral thalamic neurons in chronic pain and non-pain patients. Pain, 80: 567-575.
94. Rainville, P., Duncan, G.H., Price, D.D., Carrier, B. and Bushnell, M.C. (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science, 277: 968-971.
95. Rainville, P., Chen, C.C. and Bushnell, M.C. (1999) Psychophysical study of noxious and innocuous cold discrimination in monkey. Exp. Brain Res., 125: 28-34.
96. Ralston III, H.J. and Ralston, D.D. (1994) Medial lemniscal and spinal projections to the macaque thalamus: An electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms. J. Neurosci., 14: 2485-2502.
97. Richardson, D.E. (1967) Thalamotomy for intractable pain. Confin. Neurol., 29: 139-145.
98. Satinoff, E. (1978) Neural organization and evolution of thermal regulation in mammals. Science, 201: 16-22.
99. Schaible, H.-G. and Schmidt, R.F. (1996) Neurobiology of articular nociceptors. In: C. Belmonte and F. Cervero (Eds.), Neurobiology of Nociceptors. Oxford University Press, Oxford, pp. 202-220.
100. Schmahmann, J.D. and Leifer, D. (1992) Parietal pseudothalamic pain syndrome: Clinical features and anatomic correlates. Arch. Neurol., 49: 1032-1037.
101. Schmelz, M., Schmidt, R., Bickel, A., Handwerker, H.O. and Torebjörk, H.E. (1997) Specific C-receptors for itch in human skin. J. Neurosci., 17: 8003-8008.
102. Schott, G.D. (1996) From thalamic syndrome to central post-stroke pain. J. Neurol. Neurosurg. Psychiatry, 61: 560-564.
103. Sherrington, C.S. (1900) Cutaneous sensations. In: E.A. Schäfer (Ed.), Text-book of Physiology. Pentland, Edinburgh, pp. 920-1001.
104. Simone, D.A., Alreja, M. and LaMotte, R.H. (1991) Psychophysical studies of the itch sensation and itchy skin ('alloknesis') produced by intracutaneous injection of histamine. Somatosens. Mot. Res., 8: 271-280.
105. Stoleru, S., Gregoire, M.C., Gerard, D., Decety, J., Lafarge, E., Cinotti, L., Lavenne, F., Le Bars, D., Vernet-Maury, E., Rada, H., Collet, C., Mazoyer, B., Forest, M.G., Magnin, F., Spira, A. and Comar, D. (1999) Neuroanatomical correlates of visually evoked sexual arousal in human males. Arch. Sex Behav., 28: 1-21.
106. Strassman, A.M., Vos, B.P., Mineta, Y., Naderi, S., Borsook, D. and Burstein, R. (1993) Fos-like immunoreactivity in the superficial medullary dorsal horn induced by noxious and innocuous thermal stimulation of facial skin in the rat. J. Neurophysiol., 70: 1811-1821.
107. Sugiura, Y., Lee, C.L. and Perl, E.R. (1986) Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science, 234: 358-361.
108. Susser, E., Sprecher, E. and Yarnitsky, D. (1999) Paradoxical heat sensation in healthy subjects: Peripherally conducted by A-delta or C fibres?. Brain, 122: 239-246.
109. Thunberg, T. (1896) Förnimmelserne vid till samma ställe lokaliserad, samtidigt pågående köld- och värmeretning. Uppsala Läkfören. Förh., 2(1): 489-495.
110. Tommerdahl, M., Delemos, K.A., Vierck Jr., C.J., Favorov, O.V. and Whitsel, B.L. (1996a) Anterior parietal cortical response to tactile and skin- heating stimuli applied to the same skin site. J. Neurophysiol., 75: 2662-2670.
111. Tommerdahl, M., Whitsel, B.L., Vierck Jr., C.J., Favorov, O., Juliano, S., Cooper, B., Metz, C. and Nakhle, B. (1996b) Effects of spinal dorsal column transection on the response of monkey anterior parietal cortex to repetitive skin stimulation. Cereb. Cortex, 6: 131-155.
112. Vallbo, A.B., Olausson, H. and Wessberg, J. (1999) Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. J. Neurophysiol., 81: 2753-2763.
113. Van den Pol, A.N. (1999) Hypothalamic hypocretin (orexin): Robust innervation of the spinal cord. J. Neurosci., 19: 3171-3182.
114. Van Hees, J. and Gybels, J. (1981) C nociceptor activity in human nerve during painful and non painful skin stimulation. J. Neurol. Neurosurg. Psychiatry, 44: 600-607.
115. Van Hoesen, G.W., Morecraft, R.J. and Vogt, B.A. (1996) Connections of the monkey cingulate cortex. In: B.A. Vogt and M. Gabriel (Eds.), Neurobiology of Cingulate Cortex and Limbic Thalamus. Birkhäuser, Basle, pp. 249-284.
116. Vierck Jr., C.J., Cannon, R.L., Fry, G., Maixner, W. and Whitsel, B.L. (1997) Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. J. Neurophysiol., 78: 992-1002.
117. Woolf, C.J., Shortland, P. and Sivilotti, L.G. (1994) Sensitization of high mechanothreshold superficial dorsal horn and flexor motor neurones following chemosensitive primary afferent activation. Pain, 58: 141-156.
118. Yarnitsky, D. and Ochoa, J.L. (1990) Release of cold-induced burning pain by block of cold-specific afferent input. Brain, 113: 893-902.
119. Yu, X.H., Zhang, E.T., Craig, A.D., Shigemoto, R., Ribeiro-daSilva, A. and De Koninck, Y. (1999) NK-1 receptor immunoreactivity in distinct morphological types of lamina I neurons of the primate spinal cord. J. Neurosci., 19: 3545-3555.