Visceral nociceptive input into the ventral posterolateral nucleus of the thalamus: A new function for the dorsal column pathway

Journal of Neurophysiology

Volumn 76, Issue 4, 1996, Pages 2661-2674

  Al Chaer, Elie D ^a   Lawand, Nada B ^a   Westlund, Karin N ^a   Willis, William D ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; INTESTINE MOTILITY; MALE; NEUROTRANSMISSION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINOTHALAMIC TRACT; THALAMUS VENTRAL NUCLEUS; VISCERAL PAIN;

EID: 0029998094     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.4.2661     Document Type: Article

References (95)

1. AIDAR, O., GEOHEGAN, W. A., AND UNGEWITTER, L. H. Splanchnic afferent pathways in the central nervous system. J. Neurophysiol. 15: 131-138, 1952.
2. ALBE-FESSSARD, D., LEVANTE, A., AND LAMOUR, Y. Origin of spinothalamic and spinoreticular pathways in cats and monkeys. Adv. Neurol. 4: 157-166, 1974a.
3. ALBE-FESSSARD, D., LEVANTE, A., AND LAMOUR, Y. Origin of spino-thalamic tract in monkeys. Brain Res. 65: 503-509, 1974b.
4. AL-CHAER, E. D., LAWAND, N. B., WESTLUND, K. N., AND WILLIS, W. D. The dorsal column (DC) is more important for visceral pain than the spinothalamic tract? Soc. Neurosci. Abstr. 21: 644, 1995.
5. AMASSIAN, V. E. Cortical representation of visceral afferents. J. Neurophysiol. 14: 433-444, 1951a.
6. AMASSIAN, V. E. Fiber groups and spinal pathways of cortically represented visceral afferents. J. Neurophysiol. 14: 445-460, 1951b.
7. AMMONS, W. S. Characteristics of spinoreticular and spinothalamic neurons with renal inputs. J. Neurophysiol. 58: 480-495, 1987.
8. AMMONS, W. S. Primate spinothalamic cell responses to ureteral occlusion. Brain Res. 496: 124-130, 1989.
9. AMMONS, W. S. Cardiopulmonary sympathetic afferent excitation of lower thoracic spinoreticular and spinothalamic neurons. J. Neurophysiol. 64: 1907-1916, 1990.
10. AMMONS, W. S., BLAIR, R. W., AND FOREMAN, R. D. Responses of primate T1-T5 spinothalamic neurons to gallbladder distension. Am. J. Physiol. 247 (Regulatory Integrative Comp. Physiol. 16): R995-R1002, 1984.
11. 5 Spinothalamic neurons projection to medial thalamus with viscerosomatic input. J. Neurophysiol. 54: 73-89, 1985.
12. ANGAUT-PETIT, D. The dorsal column system. II. Functional properties and bulbar relay of the postsynaptic fibres of the cat's fasciculus gracilis. Exp. Brain Res. 22: 471-493, 1975.
13. APKARIAN, A. V. AND HODGE, C. J. J. The primate spinothalamic pathways. I. A quantitative study of the cells of origin of the spinothalamic pathway. J. Comp. Neurol. 288: 447-473, 1989a.
14. APKARIAN, A. V. AND HODGE, C. J. J. The primate spinothalamic pathways. II. The cells of origin of the dorsolateral and ventral spinothalamic pathways. J. Comp. Neurol. 288: 474-492, 1989b.
15. APPLEBAUM, A. E., BEALL, J. E., FOREMAN, R. D., AND WILLIS, W. D. Organization and receptive fields of primate spinothalamic tract neurons. J. Neurophysiol. 38: 572-586, 1975.
16. APPLEBAUM, A. E., LEONARD, R. B., KENSHALO, D. R., MARTIN, R. F., AND WILLIS, W. D. Nuclei in which functionally identified spinothalamic tract neurons terminate. J. Comp. Neurol. 188: 575-584, 1979.
17. ARMOUR, D. On the surgery of the spinal cord and its membranes. Lancet 2: 691-697, 1927.
18. BECK, P. W. AND HANDWERKER, H. O. Bradykinin and serotonin effects on various types of cutaneous nerve fibers. Pfluegers Arch. 347: 209-221, 1974.
19. BERKLEY, K. J., GUILBAUD, G., BENOIST, J., AND GAUTRON, M. Responses of neurons in and near the thalamic ventrobasal complex of the rat to stimulation of uterus, cervix, vagina, colon, and skin. J. Neurophysiol. 69: 557-568, 1993.
20. BERKLEY, K. J. AND HUBSCHER, C. H. Are there separate central nervous system pathways for touch and pain? Nature Med. 1: 766-773, 1995.
21. BLOOMFIELD, A. L. AND POLLAND, W. S. Experimental referred pain from the gastrointestinal tract. I. Stomach, duodenum and colon. J. Clin. Invest. 10: 453-473, 1931.
22. 5 spinothalamic tract neurons. J. Neurophysiol. 61: 573-588, 1989.
23. BROWN-SEQUARD, E. Lectures on the physiology and pathology of the central nervous system and on the treatment of organic nervous affections. Lancet 2: 593-823, 1868.
24. BRÜGGEMANN, J., SHI, T., AND APKARIAN, A. V. Squirrel monkey lateral thalamus. II. Viscero-somatic convergent representation of urinary bladder, colon and esophagus. J. Neurosci. 14: 6796-6814, 1994.
25. BURTON, M. B. AND GEBHART, G. F. Effects of intracolonic acetic acid on responses to colorectal distension in the rat. Brain Res. 672: 77-82, 1995.
26. CADWALADER, W. B. AND SWEET, J. E. Experimental work on the function of the anterolateral column of the spinal cord. J. Am. Med. Assoc. 56: 1490-1493, 1912.
27. CARSTENS, E. AND TREVINO, D. L. Laminar origins of spinothalamic projections in the cat as determined by the retrograde transport of horseradish peroxidase. J. Comp. Neurol. 182: 151-166, 1978.
28. CHANDLER, M. J., HOBBS, S. F., FU, Q.-G., KENSHALO, D. R., BLAIR, R. W., AND FOREMAN, R. D. Responses of neurons in ventroposterolateral nucleus of primate thalamus to urinary bladder distension. Brain Res. 571: 26-34, 1992.
29. CHUNG, J. M., KENSHALO, D. R. J., GERHART, K. D., AND WILLIS, W. D. Excitation of primate spinothalamic neurons by cutaneous C-fiber volleys. J. Neurophysiol. 42: 1354-1369, 1979.
30. CLIPPER, K. D. AND GIESLER, G. J. J. Postsynaptic dorsal column pathway of the rat. III. Distribution of ascending afferent fibers. J. Neurosci. 9: 3146-3168, 1989.
31. CLIPPER, K. D., HASEGAWA, T., AND WILLIS, W. D. Responses of neurons in the gracile nucleus of cats to innocuous and noxious stimuli: basic characterization and antidromic activation from the thalamus. J. Neurophysiol. 68: 818-832, 1992.
32. CRAIG, A. D., LININGTON, A. J., AND KNIFFKI, K. D. Cells of origin of spinothalamic projections to medial and/or lateral thalamus in the cat. J. Comp. Neurol. 289: 568-585, 1989.
33. DAVIDOFF, R. A. The dorsal columns. Neurology 39: 1377-1385, 1989.
34. DAVIS, K. D. AND DOSTROVSKY, J. O. Properties of feline thalamic neurons activated by stimulation of the middle meningeal artery and sagittal sinus. Brain Res. 454: 89-100, 1988.
35. DAVIS, K. D., TASKER, R. R., KISS, Z. H. T., HUTCHISON, W. D., AND DOSTROVSKY, J. O. Visceral pain evoked by thalamic microstimulation in humans. Neuroreport 6: 369-374, 1995.
36. DELL, P. AND OLSON, R. Projections thalamiques, corticales et cerebelleuses des afferences viscerales vagales. Soc. Biol. 145: 1084-1088, 1951.
37. DOBRY, P. J. K. AND CASEY, K. L. Roughness discrimination in cats with dorsal column lesions. Brain Res. 44: 385-397, 1972.
38. EMMERS, R. Separate relays of tactile, pressure, thermal, and gustatory modalities in the cat thalamus. Proc. Soc. Exp. Biol. Med. 121: 527-531, 1966.
39. FERRINGTON, D. G., DOWNIE, J. W., AND WILLIS, W. D. Primate nucleus gracilis neurons: responses to innocuous and noxious stimuli. J. Neurophysiol. 59: 886-907, 1988.
40. FOREMAN, R. D., BLAIR, R. W., AND WEBER, R. N. Viscerosomatic convergence onto T2-T4 spinoreticular, spinoreticular-spinothalamic, and spinothalamic tract neurons in the cat. Exp. Neurol. 85: 597-619, 1984.
41. FOREMAN, R. D., HANCOCK, M. B., AND WILLIS, W. D. Responses of spinothalamic tract cells in the thoracic spinal cord of the monkey to cutaneous and visceral inputs. Pain 11: 149-162, 1981.
42. GEBHART, G. F. AND SENGUPTA, J. N. Evaluation of visceral pain. In: Handbook of Methods in Gastrointestinal Pharmacology, edited by T. S. Gaginella. New York: CRC, 1996, p. 359-373.
43. GIESLER, G. J. J., MENÉTREY, D., AND BASBAUM, A. I. Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat. J. Comp. Neurol. 184: 107-126, 1979.
44. GIESLER, G. J. J., MENÉTREY, D., GUILBAUD, G., AND BESSON, J. Lumbar cord neurons at the origin of the spinothalamic tract in the rat. Brain Res. 118: 320-324, 1976.
45. GILDENBERG, P. L. AND HIRSHBERG, R. M. Limited myelotomy for the treatment of intractable cancer pain. J. Neurol. Neurosurg. Psychiatry 47: 94-96, 1984.
46. GLENDINNING, D. S. AND VIERCK, C. J. J. Lack of a proprioceptive deficit after dorsal column lesions in monkeys. Neurology 43: 363-366, 1993.
47. GYBELS, J. M. AND SWEET, W. H. Neurosurgical treatment of persistent pain. Physiological and pathological mechanisms of human pain. Basel: Karger, p. 1-442, 1989.
48. HABLER, H.-J., JÄNIG, W., AND KOLTZENBURG, M. A novel type of unmyelinated chemosensitive nociceptor in the acutel inflamed urinary bladder. Agents Actions 25: 219-221, 1988.
49. HANCOCK, M. B., FOREMAN, R. D., AND WILLIS, W. D. Convergence of visceral and cutaneous input onto spinothalamic tract cells in the thoracic spinal cord of the cat. Exp. Neurol. 47: 240-248, 1975.
50. HEAD, H. AND THOMPSON, T. The grouping of afferent impulses within the spinal cord. Brain 29: 537-741, 1906.
51. HIRSHBERG, R. M., AL-CHAER, E. D., LAWAND, N. B., WESTLUND, K. N., AND WILLIS, W. D. Is there a pathway in the dorsal funiculus that signals visceral pain? (Abstract) 10th Eur. Congr. Neurosurg. Berlin 1995.
52. HITCHCOCK, E. R. Stereotactic cervical myelotomy. J. Neurol. Neurosurg. Psychiatry 33: 224-230, 1970.
53. HITCHCOCK, E. R. Stereotactic myelotomy. Proc. R. Soc. Med. 67: 771-772, 1974.
54. 6 spinothalamic tract cells of the monkey. J. Neurophysiol. 68: 1575-1588, 1992.
55. HURST, A. F. The sensibility of the alimentary canal in health and diseases (Abstract). Lancet 1: 1051, 1911.
56. KEVETTER, G. A. AND WILLIS, W. D. Spinothalamic cells in the rat lumbar cord with collaterals to the medullary reticular formation. Brain Res. 238: 181-185, 1982.
57. KUO, D. C. AND DE GROAT, W. C. Primary afferent projections of the major splanchnic nerve to the spinal cord and the nucleus gracilis of the cat. J. Comp. Neurol. 231: 421-434, 1985.
58. LAURITSEN, K., LAURSEN, L., BUKHAVE, K., AND RASK-MADSEN, J. In vivo profiles of eicosanoids in ulcerative colitis and Clostridium difficile colitis. Gastroenterology 95: 11-17, 1988.
59. LAWAND, N. B., AL-CHAER, E. D., WESTLUND, K. N., AND WILLIS, W. D. Administration of morphine and CNQX in the rat sacral cord blocks the responses of dorsal column nuclei (DCN) cells to visceral but not to cutaneous stimulation Soc. Neurosci. Abstr. 21: 644, 1995.
60. LIPKIN, M. AND SLIESENGER, M. H. Studies of visceral pain: measurements of stimulus intensity and duration associated with the onset of pain in esophagus, ileum and colon. J. Clin. Invest. 37: 28-34, 1958.
61. MCLEOD, J. G. The representation of the splanchnic afferent pathways in the thalamus of the cat. J. Physiol. Lond. 94: 439-452, 1958.
62. MCMAHON, S. B. AND ABEL, C. A model for the study of visceral pain states: chronic inflammation of the chronic decerebrate rat urinary bladder by irritant chemicals. Pain 28: 109-127, 1987.
63. MILNE, R. J., FOREMAN, R. D., GIESLER, G. J. J., AND WILLIS, W. D. Convergence of cutaneous and pelvic visceral nociceptive inputs onto primate spinothalamic neurons. Pain 11: 163-183, 1981.
64. MILNE, R. J., FOREMAN, R. D., AND WILLIS, W. D. Responses of primate spinothalamic neurons located in the sacral intermediolateral gray (Stilling's nucleus) to proprioceptive input from the tail. Brain Res. 234: 227-236, 1982.
65. NESS, T. J. AND GEBHART, G. F. Characterization of neuronal responses to noxious visceral and somatic stimuli in the medial lumbosacral spinal cord of the rat. J. Neurophysiol. 57: 1867-1892, 1987.
66. NESS, T. J. AND GEBHART, G. F. Characterization of neurons responsive to noxious colorectal distension in the T13-L2 spinal cord of the rat. J. Neurophysiol. 60: 1419-1438, 1988a.
67. NESS, T. J. AND GEBHART, G. F. Colorectal distension as a noxious visceral stimulus: physiologic and pharmacologic characterization of pseudaffective reflexes in the rat. Brain Res. 450: 153-169, 1988b.
68. NESS, T. J., METCALF, A. M., AND GEBHART, G. F. A psychophysiological study in humans using phasic colonic distension as a noxious visceral stimulus. Pain 43: 377-386, 1990.
69. PATTON, H. D. AND AMASSIAN, V. E. Thalamic relay of splanchnic afferent fibers. Am. J. Physiol. 167: 815-816, 1951.
70. PESCHANSKI, M., BRIAND, A., GAUTRON, M., AND GUILBAUD, G. Electrophysiological evidence for a role of the anterolateral quadrant of the spinal cord in the transmission of noxious messages to the thalamic ventrobasal complex in the rat. Brain Res. 342: 77-84, 1985.
71. PITCHFORD, S. AND LEVINE, J. D. Prostaglandins sensitize nociceptors in cell culture. Neurosci. Lett. 132: 105-108, 1991.
72. RIGAMONTI, D. D. AND HANCOCK, M. B. Analysis of field potentials elicited in the dorsal column nuclei by splanchnic nerve A-beta afferents. Brain Res. 77: 326-329, 1974.
73. RIGAMONTI, D. D. AND HANCOCK, M. B. Viscerosomatic convergence in the dorsal column nuclei. Exp. Neurol. 61: 337-348, 1978.
74. RITCHIE, J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 14: 125-132, 1973.
75. ROGERS, R. C., NOVIN, D., AND BUTCHER, L. L. Hepatic sodium and osmoreceptors activate neurons in the ventrobasal thalamus. Brain Res. 168: 398-403, 1979.
76. RUCKER, H. K., HOLLOWAY, J. A., AND KEYSER, G. F. Response chracteristics of cat spinothalamic tract neurons to splanchnic nerve stimulation. Brain Res. 291: 383-387, 1984.
77. RUSTIONI, A. Non-primary afferents to the nucleus gracilis from the lumbar cord of the cat. Brain Res. 51: 81-95, 1973.
78. SARNOFF, S. J., ARROWOOD, J. G., AND CHAPMAN, W. P. Differential spinal block. IV. The investigation of intestinal dyskinesia, colonic atony, and visceral afferent fibers. Surg. Gynecol. Obstet. 86: 571-581, 1948.
79. SCHVARCZ, J. R. Stereotactic extralemniscal myelotomy. J. Neurol. Neurosurg. Psychiatry 39: 53-57, 1976.
80. SENGUPTA, J. N. AND GEBHART, G. F. Characterization of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat. J. Neurophysiol. 71: 2046-2060, 1994.
81. SPILLER, W. G. AND MARTIN, E. The treatment of persistent pain of organic origin in the lower part of the body by division of the anterolateral column of the spinal cord. J. Am. Med. Assoc. 58: 1489-1490, 1912.
82. STANLEY, E. A case of disease of the posterior columns of the spinal cord. Med-chir. Trans. 23: 80-84, 1840.
83. TREVINO, D. L., COULTER, J. D., AND WILLIS, W. D. Locations of cells of origin of spinothalamic tract in lumbar enlargement of the monkey. J. Neurophysiol. 36: 750-761, 1973.
84. TREVINO, D. L., MAUNZ, R. A., BRYAN, R. N., AND WILLIS, W. D. Location of cells of origin of the spinothalamic tract in the lumbar enlargement of cat. Exp. Neurol. 34: 64-77, 1972.
85. VIERCK, C. J. J., COHEN, R. H., AND COOPER, B. Y. Effects of spinal lesions on temporal resolution of cutaneous sensations. Somatosens. Res. 3: 45-56, 1985.
86. VIERCK, C. J. J., FAVOROV, O., AND WHITSEL, B. L. Neural mechanisms of absolute tactile localization in monkeys. Somatosens. Res. 6: 41-62, 1988.
87. VIERCK, C. J. J. AND LUCK, M. M. Loss and recovery of reactivity to noxious stimuli in monkeys with primary spinothalamic cordotomies, followed by secondary and tertiary lesions of other cord sectors. Brain 102: 233-248, 1979.
88. VIERCK, C. J. J. AND RAND, R. Localization of touch on glabrous skin following dorsal column lesion in a primate. Soc. Neurosci. Abstr. 5: 715, 1979.
89. WALDRON, D. J., GILL, R. C., AND BOWES, K. L. Pressure responses of human colon to intraluminal distension. Dig. Dis. Sci. 34: 1163-1167, 1989.
90. WHITE, J. C. Sensory innervation of the viscera: studies on visceral afferent neurones in man based on neurosurgical procedures for the relief of intractable pain. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 23: 373-390, 1943.
91. WHITE, J. C. AND SWEET, W. H. Pain and the neurosurgeon. A forty-year experience. Springfield, IL: Charles C Thomas, p. 1-1000, 1969.
92. WILLIS, W. D. AND COGGESHALL, R. E. Sensory Mechanisms of the Spinal Cord. New York: Plenum, 1991,.
93. WILLIS, W. D., KENSHALO, D. R. J., AND LEONARD, R. B. The cells of origin of the primate spinothalamic tract. J. Comp. Neurol. 188: 543-574, 1979.
94. WILLIS, W. D., TREVINO, D. L., COULTER, J. D., AND MAUNZ, R. A. Responses of primate spinothalamic tract neurons to natural stimulation of the himdlimb. J. Neurophysiol. 37: 358-372, 1974.
95. WOODWORTH, R. S. AND SHERRINGTON, C. S. A pseudaffective reflex and its spinal path. J. Physiol. Lond. 31: 234-243, 1904.