Serotonergic neural precursor cell grafts attenuate bilateral hyperexcitability of dorsal horn neurons after spinal hemisection in rat

Neuroscience

Volumn 116, Issue 4, 2003, Pages 1097-1110

  Hains, B C ^a,b   Johnson, K M ^a   Eaton, M J ^c   Willis, W D ^a   Hulsebosch, C E ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Electrophysiology; Hemisection; Nociception; Pain; Spinal cord injury; Transplantation

Indexed keywords

METHYSERGIDE; NEUROTROPHIC FACTOR; SEROTONIN;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CELL TRANSPLANTATION; CHRONIC PAIN; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED SPINAL CORD RESPONSE; EXPERIMENTAL MODEL; HYPERALGESIA; LUMBAR SPINAL CORD; MALE; MECHANORECEPTOR; NERVE EXCITABILITY; NERVE GRAFT; NEUROANATOMY; NOCICEPTION; NOCICEPTIVE RECEPTOR; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SEROTONIN RELEASE; SEROTONINERGIC NERVE CELL; SPECIES COMPARISON; SPIKE; SPINAL CORD DORSAL HORN; SPINAL CORD HEMISECTION; SPINAL CORD INJURY; SPINAL CORD NERVE CELL; STEM CELL; STIMULUS RESPONSE; THORACIC SPINAL CORD;

EID: 0037470570     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00729-7     Document Type: Article

References (121)

1. Baba H., Kohno T., Moore K.A., Woolf C.J. Direct activation of rat spinal dorsal horn neurons by prostaglandin E2. J Neurosci. 21:2001;1750-1756.
2. Barbaro N.M., Hammond D.L., Fields H.L. Effects of intrathecally administered methysergide and yohimbine on microstimulation-produced antinociception in the rat. Brain Res. 343:1985;223-229.
3. Bardin L., Bardin M., Lavarenne J., Eschalier A. Effect of intrathecal serotonin on nociception in rats influence of the pain test used . Exp Brain Res. 113:1997;81-87.
4. Basbaum A.I. Conduction of the effects of noxious stimulation by short-fiber multisynaptic systems of the spinal cord in rat. Exp Neurol. 40:1973;699-716.
5. Basbaum A.I., Fields H.L. Endogenous pain control mechanisms review and hypothesis . Ann Neurol. 4:1979;451-462.
6. Basbaum A.I., Fields H.L. Endogenous pain systems brainstem pathways and endorphin circuitry . Annu Rev Neurosci. 7:1984;309-338.
7. Basbaum A.I., Wall P.D. Chronic changes in the response of cells in adult cat dorsal horn following partial deafferentation the appearance of responding cells in a previously non-responding region . Brain Res. 116:1976;181-204.
8. Basso D.M., Beattie M.S., Bresnahan J.C. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma. 12:1995;1-21.
9. Bennett G.J., Xie Y.K. A peripheral motoneuropathy in rat that produces disorders of pain sensation like those seen in man. Pain. 33:1988;87-107.
10. Besson J.M., Chaouch A. Descending serotoninergic systems. Pain Headache. 9:1987;64-100.
11. Besson J.M., Oliveras J.L., Chaouch A., Rivot J.P. Role of the raphe nuclei in stimulation producing analgesia. Adv Exp Med Biol. 133:1981;153-176.
12. Bowsher D. Contralateral mirror-image pain following anterolateral cordotomy. Pain. 33:1988;63-65.
13. Brewer K.L., Yezierski R.P. Effects of adrenal medullary transplants on pain-related behaviors following excitotoxic spinal cord injury. Brain Res. 798:1998;83-92.
14. Burchiel J.J. Spontaneous impulse generation in normal and denervated dorsal root ganglia sensitivity to alpha-adrenergic stimulation and hypoxia . Exp Neurol. 85:1984;257-272.
15. Cejas M., Martinez M., Karmally S., Mckillop M., Mckillop J., Plunkett J.A., Oudega M., Eaton M.J. Lumbar transplant of neurons genetically modified to secrete brain-derived neurotrophic factor attenuates allodynia and hyperalgesia after sciatic nerve constriction. Pain. 86:2000;195-210.
16. Choi Y., Yoon Y.W., Na H.S., Kim S.H., Chung J.M. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain. 59:1994;369-376.
17. Christensen M.D., Everhart A.W., Pickelmann J.T., Hulsebosch C.E. Mechanical and thermal allodynia in chronic central pain following spinal cord injury. Pain. 68:1996;97-107.
18. Christensen M.D., Hulsebosch C.E. Chronic central pain after spinal cord injury. J Neurotrauma. 14:1997;517-537.
19. Chung J.M., Lee K.H., Surmeier D.J., Sorkin L.S., Kim J., Willis W.D. Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J Neurophysiol. 56:1986;370-390.
20. Chung K., Chung J.M. Sympathetic involvement in the spinal nerve ligation model of neuropathic pain. Harden R.N., Baron R., Janig W. Complete regional pain syndrome: Progress in pain research and management. 2001;1-8 IASP Press, Seattle, WA.
21. Cirulli F., Berry A., Alleva E. Intracerebroventricular administration of brain-derived neurotrophic factor in adult rats affects analgesia and spontaneous behavior but not memory retention in a Morris Water Maze task. Neurosci Lett. 287:2000;207-210.
22. Coggeshall R.E., Lekan H.A., White F.A., Woolf C.J. A-fiber sensory inputs induces neuronal cell death in the dorsal horn of the adult rat spinal cord. J Comp Neurol. 435:2001;276-282.
23. Clarke R.W., Ogilvie J., Houghton A.K. Enhancement and depression of spinal reflexes by 8-hydroxy-2-(di-n-propylamino)tetralin in the decerebrated and spinalized rabbit involvement of 5-HT1A- and non-5-HT1A-receptors . Br J Pharmacol. 122:1997;631-638.
24. Cowley K.C., Schmidt B.J. Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J Neurophysiol. 77:1997;247-259.
25. Crick H., Manuel N.A., Wallis D.I. A novel 5-HT receptor or a combination of 5-HT receptor subtypes may mediate depression of a spinal monosynaptic reflex in vitro. Neuropharmacology. 33:1994;897-904.
26. Culbertson J.L., Hines D.E., Kimmel D.L., Brown P.B. Contralateral projection of primary afferent fibers to mamallian spinal cord. Exp Neurol. 64:1979;83-97.
27. Dado R.J., Katter J.T., Giesler G.J. Spinothalamic and spinohypothalamic tract neurons in the cervical enlargement of rats. II. Responses to innocuous and noxious mechanical stimuli. J Neurophysiol. 71:1994;981-1002.
28. Devor M., Wall P.D. Effect of peripheral nerve injury on receptive fields of cells in the cat spinal cord. J Comp Neurol. 199:1981;277-291.
29. Dirig D.M., Salami A., Rathbun M.L., Ozaki G.T., Yaksh T.L. Characterization of variables defining hindpaw withdrawal latency evoked by radiant thermal stimuli. J Neurosci Meth. 76:1997;183-191.
30. Dougherty P.M., Sluka K.A., Sorkin L.S., Westlund K.N., Willis W.D. Neural changes in acute arthritis in monkeys. I. Parallel enhancement of responses of spinothalamic tract neurons to mechanical stimulation and excitatory amino acids Brain Res Rev. 17:1992;1-13.
31. Dougherty P.M., Staats P.S. Intrathecal drug therapy for chronic pain from basic science to clinical practice . Anesthesiology. 9:1999;891-918.
32. Dougherty P.M., Willis W.D. Modification of the responses of primate spinothalamic neurons to mechanical stimulation by excitatory amino acids and an N-methyl-D-aspartate antagonist. Brain Res. 542:1991;15-22.
33. Dougherty P.M., Willis W.D. Enhanced responses of spinothalamic tract neurons to excitatory amino acids accompany capsaicin-induced sensitization in the monkey. J Neurosci. 12:1992;883-894.
34. Downie J.W., Ferrington D.G., Sorkin L.S., Willis W.D. The primate spinocervicothalamic pathway responses of cells of the lateral cervical nucleus and spinocervical tract to innocuous and noxious stimuli . J Neurophysiol. 59:1988;861-885.
35. Drew G.M., Siddall P.J., Duggan A.W. Responses of spinal neurons to cutaneous and dorsal root stimuli in rats with mechanical allodynia after contusive spinal cord injury. Brain Res. 893:2001;59-69.
36. Dubner R. Neuronal plasticity and pain following peripheral tissue inflammation or nerve injury. In: Proceedings of the VIth World Congress on Pain. 1991;Elsevier, Amsterdam.
37. Eaton M.J., Martinez M., Karmally S., Lopez T., Sagen J. Initial characterization of the transplant of immortalized chromaffin cells for the attenuation of chronic neuropathic pain. Cell Transplant. 9:2000;637-656.
38. Eaton M.J., Santiago D.L., Dancausse H.A., Whittemore S.R. Lumbar transplants of immortalized serotonergic neurons alleviate chronic neuropathic pain. Pain. 72:1997;59-69.
39. Eaton M.J., Whittemore S.R. Autocrine BDNF secretion enhances the survival and serotonergic differentiation of raphe neuronal precursor cells grafted into the adult rat. Exp Neurol. 140:1996;105-114.
40. Griesbeck O., Canossa M., Campana G., Gartner A., Hoener M.C., Nawa H., Kolbech R., Thoenen H. Are there differences between the secretion characteristics of NGF and BDNF? Implications for the modulatory role of neurotrophins in activity-dependent neuronal plasticity Microsc Res Tech. 45:1999;262-275.
41. Hains B.C., Chastain K.M., Everhart A.W., Hulsebosch C.E. Transplants of adrenal medullary chromaffin cells reduce forelimb and hindlimb allodynia in a rodent model of chronic central pain after spinal cord hemisection injury. Exp Neurol. 164:2000;426-437.
42. Hains B.C., Fullwood S.D., Eaton M.J., Hulsebosch C.E. Subdural engraftment of serotonergic neurons following spinal hemisection restores spinal serotonin, downregulates serotonin transporter, and increases BDNF tissue content in rat. Brain Res. 913:2001;35-46.
43. Hains B.C., Johnson K.M., McAdoo D.J., Eaton M.J., Hulsebosch C.E. Engraftment of immortalized serotonergic neurons enhances locomotor function and attenuates chronic central pain following spinal hemisection injury in the rat. Exp Neurol. 171:2001;361-378.
44. Hains B.C., Willis W.D., Hulsebosch C.E. Differential electrophysiological effects of brain-derived neurotrophic factor on dorsal horn neurons following chronic spinal cord hemisection injury in the rat. Neurosci Lett. 320:2002;125-128.
45. Hains B.C., Everhart A.W., Hulsebosch C.E. Changes in serotonin, serotonin transporter expression and serotonin denervation supersensitivity involvement in chronic central pain after spinal hemisection in the rat . Exp Neurol. 75:2002;347-362.
46. 3 mediate hyperexcitability of wide dynamic range dorsal horn neurons after chronic spinal cord hemisection injury in rat. Exp Brain Res. 2002;. in press.
47. Hao J.X., Xu X.J., Yu Y.X., Seiger A., Wiesenfeld-Hallin Z. Transient spinal cord ischemia induces temporary hypersensitivity of dorsal horn wide dynamic range neurons to myelinated, but not unmyelinated, fiber input. J Neurophysiol. 68:1992;384-391.
48. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 32:1988;77-88.
49. Hentall I.D., Sagen J. The alleviation of pain by cell transplantation. Prog Brain Res. 127:2000;535-550.
50. Hentall I.D., Noga B.R., Sagen J. Spinal allografts of adrenal medulla block nociceptive facilitation in the dorsal horn. J Neurophysiol. 85:2001;1788-1792.
51. Hulsebosch C.E., Hains B.C., Waldrep K., Young W. Bridging the gap from discovery to clinical trials in spinal cord injury . J Neurotrauma. 17:2000;1117-1128.
52. Hulsebosch C.E., Xu G.Y., Perez-Polo J.R., Westlund K.N., Taylor C.P., McAdoo D.J. Rodent model of chronic central pain after spinal cord contusion injury and effects of gabapentin. J Neurotrauma. 17:2000;1205-1217.
53. Ji R.-R., Befort K., Brenner G.J., Woolf C.J. ERK MAP Kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci. 22:2002;478-485.
54. Kerr B.J., Bradbury E.J., Bennett D.L.H., Trivedi P.M., Dassan P., French J., Shelton D.B., McMahon S.B., Thompson W. Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J Neurosci. 19:1999;6138-6148.
55. Koerber H.R., Mirnics K., Brown P.R., Mendell L.M. Central sprouting and functional plasticity of regenerated primary afferents. J Neurosci. 14:1994;3655-3671.
56. Krenz N.R., Weaver L.C. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neurosciences. 85:1998;443-458.
57. Lazorthes Y., Sagen J., Sallerin B., Tkaczuk J., Duplan H., Sol J.C., Tafani M., Bes J.C. Human chromaffin cell graft into the CSF for cancer pain management a prospective phase II clinical study . Pain. 87:2000;19-32.
58. Levitt M. Dysesthesias and self-mutilation in humans and subhumans a review of clinical and experimental studies . Brain Res Rev. 10:1985;247-290.
59. Levitt M. The theory of chronic deafferentation dysesthesias. J Neurosurg Soc. 34:1990;71-98.
60. Li H., Lang B., Kang J.F., Li Y.Q. Serotonin potentiates the response of neurons of the superficial laminae of the rat spinal dorsal horn to gamma-aminobutyric acid. Brain Res Bull. 52:2000;559-565.
61. Liebeskind J.C., Guilbaud G., Besson J.M., Oliveras J.L. Analgesia from electrical stimulation of the periaqueductal gray matter in the cat behavioral observations and inhibitory effects on spinal cord interneurons . Brain Res. 50:1973;441-446.
62. Light A.R., Perl E.R. Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol. 186:1979;133-150.
63. Lin Q., Peng Y.B., Willis W.D. Antinociception and inhibition from the periaqueductal gray are mediated in part by spinal 5-hydroxytryptamine(1A) receptors. J Pharmacol Exp Ther. 276:1996;958-967.
64. Lindsey A.E., LoVerso R.L., Tovar C.A., Hill C.E., Beattie M.S., Bresnahan J.C. An analysis of changes in sensory thresholds to mild tactile and cold stimuli after experimental spinal cord injury in the rat. Neurorehabil Neural Repair. 14:2000;287-300.
65. Liu C.N., Chambers W.W. Intraspinal sprouting of dorsal root axons. Arch Neurol Psychiatry. 79:1958;46-61.
66. Loeser J.D., Ward A.A., White L.E. Chronic deafferentation of human spinal cord neurons. J Neurosurg. 29:1968;48-50.
67. Lombard M.C., Nashold B.S., Albe-Fessard D. Deafferentation hypersensitivity in the rat after dorsal rhizotomy possible animal model for chronic pain . Pain. 6:1979;163-174.
68. Mannion R.J., Costigan M., Decosterd I., Amaya F., Ma Q.P., Holstege J.C., Ji R.R., Acheson A., Lindsay R.M., Wilkinson G.A., Woolf C.J. Neurotrophins peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity . Proc Natl Acad Sci U S A. 96:1999;9385-9390.
69. McNeill D.L., Carlton S.M., Hulsebosch C.E. Intraspinal sprouting of calcitonin gene-related peptide containing primary afferents after deafferentation in the rat. Exp Neurol. 114:1991;321-329.
70. Melzack R., Loeser J.D. Phantom body pain in paraplegics evidence for a central "pattern generating mechanism" for pain . Pain. 4:1978;195-210.
71. Mendell L.M. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol. 16:1966;316-332.
72. Mercadante M.S. Problems of long-term spinal opioid treatment in advanced cancer pain. Pain. 79:1999;1-13.
73. Miki K., Fukuoka T., Tokunaga A., Kondom E., Dai Y., Noguchi K. Differential effect of brain-derived neurotrophic factor on high-threshold mechanosensitivity in a rat neuropathic pain model. Neurosci Lett. 278:2000;85-88.
74. Miki K., Fukuoka T., Tokunaga A., Noguchi K. Calcitonin gene-related peptide increase in the rat spinal dorsal horn and dorsal column nucleus following peripheral nerve injury up-regulation in a subpopulation of primary afferent sensory neurons . Neuroscience. 82:1998;1243-1252.
75. Miller S., Van Der Burg J., Van Der Meche F. Coordination of movements of the hindlimbs and forelimbs in different forms of locomotion in normal and decerebrate cats. Brain Res. 91:1975;217-237.
76. Mills C.D., Fullwood S.D., Hulsebosch C.E. Changes in metabotropic glutamate receptor expression following spinal cord injury in rat. J Neurotrauma. 170:2001;244-257.
77. Murray M., Goldberger M.E. Restitution of function and collateral sprouting in the cat spinal cord the partially hemisected animal . J Comp Neurol. 158:1974;19-36.
78. Murray M., Goldberger M.E. Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral umbosacral dorsal rhizotomy in adult cats. J Neurosci. 6:1986;3205-3217.
79. Nakagawa I., Omote K., Kitahata L.M., Collins J.G., Murata K. Serotonergic mediation of spinal analgesia and its interaction with noradrenergic systems. Anesthesiology. 73:1990;474-478.
80. Nakata Y., Kusaka Y., Segawa T. Supersensitivity to substance P after dorsal root section. Life Sci. 24:1979;1651-1654.
81. Oudega M., Blits B., Ruitenberg M.J., Karmaly S., Verhaagen J., Eaton M.J. Amelioration of chronic neuropathic pain by adeno-associated viral vector-mediated overexpression of BDNF in the rat spinal cord. Soc Neurosci Abs. 26:2000;1692.
82. Owens C.M., Zhang D., Willis W.D. Changes in the response states of primate spinothalamic tract cells caused by mechanical damage of the skin or activation of descending controls. J Neurophysiol. 67:1992;1509-1527.
83. Oyelese A.A., Rizzo M.A., Waxman S.G., Kocsis J.D. Differential effects of NGF and BDNF on axotomy-induced changes in GABA(A)-receptor-mediated conductance and sodium currents in cutaneous afferent neurons. J Neurophysiol. 78:1997;31-42.
84. Paik K.S., Gwak Y.S., Yeon D.S., Leem J.W., Nam T.S. Modulation of response properties of spinal dorsal horn neurons following spinal cord injury in rat. Soc Neurosci Abs. 26:2000;1690.
85. Palecek J., Dougherty P.M., Kim S.H., Paleckova V., Lekan H., Chung J.M., Carlton S.M., Willis W.D. Responses of spinothalamic tract neurons to mechanical and thermal stimuli in an experimental model of peripheral neuropathy in primates. J Neurophysiol. 68:1992;1951-1966.
86. Palecek J., Paleckova V., Dougherty P.M., Carlton S.M., Willis W.D. Responses of spinothalamic tract cells to mechanical and thermal stimulation of skin in rats with experimental peripheral neuropathy. J Neurophysiol. 67:1992;1562-1573.
87. Peng Y.B., Lin Q., Willis W.D. The role of 5-HT3 receptors in periaqueductal gray-induced inhibition of nociceptive dorsal horn neurons in rats. J Pharmacol Exp Ther. 276:1996;116-124.
88. Peng Y.B., Lin Q., Willis W.D. Involvement of protein kinase C in responses of rat dorsal horn neurons to mechanical stimuli and periaqueductal gray descending inhibition. Exp Brain Res. 114:1997;561-570.
89. Peng Y.B., Wu J., Willis W.D., Kenshalo D.R. GABA(A) and 5-HT(3) receptors are involved in dorsal root reflexes possible role in periaqueductal gray descending inhibition . J Neurophysiol. 86:2001;49-58.
90. Polistina D.C., Murray M., Goldberger M.E. Plasticity of dorsal root descending serotonergic projections after partial deafferentation of the adult rat spinal cord. J Comp Neurol. 299:1990;349-363.
91. Qin C., Chandler M.J., Miller K.E., Foreman R.D. Chemical activation of cervical cell bodies effects on responses to colorectal distension in lumbosacral spinal cord of rats . J Neurophysiol. 82:1999;3423-3433.
92. Reynolds D.V. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science. 164:1969;444-445.
93. Rutherford L.C., Nelson S.B., Turrigiano G.G. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron. 21:1998;521-530.
94. Sagen J., Pappas G.D., Pollard H.B. Analgesia induced by isolated bovine chromaffin cells implanted in rat spinal cord. Proc Natl Acad Sci U S A. 83:1986;7522-7526.
95. Saruhashi Y., Young W., Perkins R. The recovery of 5-HT immunoreactivity in lumbosacral spinal cord and locomotor function after thoracic hemisection. Exp Neurol. 139:1996;203-213.
96. Simone D.A., Sorkin L.S., Oh U., Chung J.M., Owens C., Lamotte R.H., Willis W.D. Neurogenic hyperalgesia central neural correlates in responses of spinothalamic tract neurons . J Neurophysiol. 66:1991;228-246.
97. Siuciak J.A., Altar C.A., Wiegand S.J., Lindsay R.M. Antinociceptive effect of brain-derived neurotrophic factor and neurotrophin-3. Brain Res. 633:1994;326-330.
98. Siuciak J.A., Wong V., Pearsall D., Wiegand S.J., Lindsay R.M. BDNF produces analgesia in the formalin test and modifies neuropeptide levels in rat brain and spinal cord areas associated with nociception. Eur J Neurosci. 7:1995;663-670.
99. Skagerberg G., Bjorklund A. Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neurosci. 15:1985;445-480.
100. Skinner R.D., Adams R.J., Remmel R.S. Responses of long descending propriospinal neurons to natural and electrical types of stimuli in cat. Brain Res. 196:1980;387-403.
101. Sweet W.H. Deafferentation syndromes in humans a general discussion . Nashold B.S. Jr, Ovelmen-Levitt J. Deafferentation pain syndromes: pathophysiology and treatment. 1991;259-290 Raven Press, New York.
102. Vera-Portocarrero L.P., Mills C.D., Ye Z., Fullwood S.D., McAdoo D.J., Hulsebosch C.E., Westlund K.N. Rapid changes in expression of glutamate transporters after spinal cord injury. Brain Res. 927:2002;104-110.
103. Vincler M., Maixner W., Vierck C.J., Light A.R. Effects of systemic morphine on escape latency and a hindlimb reflex response in rat. J Pain. 2:2001;83-90.
104. Wall P.D., Devor M. Sensory afferent impulses originate from dorsal root ganglia as well as from the periphery in normal and nerve injured rats. Pain. 17:1983;321-339.
105. Waxman S.G., Cummins T.R., Dib-Hajj S.D., Black J.A. Voltage-gated sodium channels and the molecular pathogenesis of pain a review . J Rehabil Res Dev. 37:2000;517-528.
106. White L.A., Eaton M.J., Castrom M.C., Klose K.J., Globus M.Y., Shaw G., Whittemorem S.R. Distinct regulatory pathways control neurofilament expression and neurotransmitter synthesis in immortalized serotonergic neurons. J Neurosci. 14:1994;6744-6753.
107. Willcockson W.S., Chung J.M., Hori Y., Lee K.H., Willis W.D. Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J Neurosci. 4:1984;732-740.
108. Willis W.D. Effects of peripherally and centrally administered serotonin on primate spinothalamic neurons. Haber B., Gabay S., Issidorides M.R., Alivisatos S.G.A. Serotonin: current aspects of neurochemistry and function. 1981;125-148 Raven Press, New York.
109. Willis W.D. Control of nociceptive transmission in the spinal cord. Ottoson D. Progress in sensory physiology. 1982;1-159 Springer-Verlag, Berlin.
110. Willis W.D. Central sensitization and plasticity following intense noxious stimulation. Mayer E.A., Raybould H.E. Basic and clinical aspects of chronic abdominal pain. 1993;Elsevier Science, Amsterdam.
111. Willis W.D., Coggeshall R.E. Sensory mechanisms of the spinal cord. 1991;Plenum Press, New York.
112. Woolf C.J. Evidence for a central component of post-injury pain hypersensitivity. Nature. 306:1983;686-688.
113. Woolf C.J. Long term alterations in the excitability of the flexion reflex produced by peripheral tissue injury in the chronic decerebrate rat. Pain. 18:1984;325-343.
114. Woolf C.J. The pathophysiology of peripheral neuropathic pain abnormal peripheral input and abnormal central processing . Acta Neurochir Suppl. 58:1993;125-130.
115. Woolf C.J., Salter M.W. Neuronal plasticity increasing the gain in pain . Science. 288:2000;1765-1768.
116. Wright D.M., Roberts M.H. Supersensitivity to a substance P analogue following dorsal root section. Life Sci. 22:1978;19-24.
117. Wu J., Fang L., Lin Q., Willis W.D. Nitric oxide synthase in spinal cord central sensitization following intradermal injection of capsaicin. Pain. 94:2001;47-58.
118. Yezierski R.P. Pain following spinal cord injury the clinical problem and experimental studies . Pain. 68:1996;185-194.
119. Yezierski R.P., Park S.H. The mechanosensitivity of spinal sensory neurons following intraspinal injections of quisqualic acid in the rat. Neurosci Lett. 57:1993;115-119.
120. Yezierski R.P., Wilcox T.K., Willis W.D. The effects of serotonin antagonists on the inhibition of primate spinothalamic tract cells produced by stimulation in nucleus raphe magnus or periaqueductal gray. J Pharmacol Exp Ther. 220:1982;266-277.
121. 3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J Neurosci. 22:2002;1010-1019.