Termination zones of functionally characterized spinothalamic tract neurons within the primate posterior thalamus

Journal of Neurophysiology

Volumn 100, Issue 4, 2008, Pages 2026-2037

  Davidson, Steve ^a   Zhang, Xijing ^a   Khasabov, Sergey G ^b   Simone, Donald A ^a,b   Giesler Jr , Glenn J ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; MACACA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD DORSAL HORN; SPINOTHALAMIC TRACT; THALAMUS POSTERIOR NUCLEUS;

ACTION POTENTIALS; ANIMALS; AXONS; BRAIN MAPPING; CAPSAICIN; COLD TEMPERATURE; DATA INTERPRETATION, STATISTICAL; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; HOT TEMPERATURE; MACACA FASCICULARIS; NEURONS; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; POSTERIOR HORN CELLS; POSTERIOR THALAMIC NUCLEI; SPINOTHALAMIC TRACTS; STIMULATION, CHEMICAL;

EID: 57349150211     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90810.2008     Document Type: Article

References (92)

1. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9: 463-484, 2005.
2. Apkarian AV, Hodge CJ. Primate spinothalamic pathways. III. Thalamic termination of the dorsolateral and ventral spinothalamic pathways. J Comp Neurol 288: 493-511, 1989.
3. Apkarian AV, Shi T. Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals. J Neurosci 14: 6779-6795, 1994.
4. Applebaum AE, Leonard RB, Kenshalo DR Jr, Martin RF, Willis WD. Nuclei in which functionally identified spinothalamic tract neurons terminate. J Comp Neurol 188: 575-586, 1979.
5. Beggs J, Jordan S, Ericson A-C, Blomqvist A, Craig AD. Synaptology of trigemino- and spinothalamic lamina I terminations in the posterior ventral medial nucleus of the Macaque. J Comp Neurol 459: 334-354, 2003.
6. Benedek G, Pereny J, Kovacs G, Fischer-Szatmari L, Katok YY. Visual, somatosensory, auditory and nociceptive modality properties in the feline suprageniculate nucleus. Neuroscience 78: 179-189, 1997.
7. Blomqvist A, Zhang ET, Craig AD. Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the posterior portion of the ventral medial nucleus, in the human thalamus. Brain 123: 601-619, 2000.
8. Boivie J. An anatomical reinvestigation of the termination of the spinothalamic tract in the monkey. J Comp Neurol 186: 343-370, 1979.
9. Bordi F, LeDoux JE. Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdale stimulation. Exp Brain Res 98: 275-286, 1994.
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 15: 37-42, 1979.
11. Burstein R, Dado RJ, Giesler GJ Jr. Physiological characterization of spinohypothalamic tract neurons in the lumbar enlargement of rats. J Neurophysiol 66: 261-284, 1991.
12. Burton H, Jones EG. The posterior thalamic region and its cortical projection in New World and Old World monkeys. J Comp Neurol 168: 249-301, 1976.
13. Bushnell MC, Duncan GH, Tremblay N. Thalamic VPM nucleus in the behaving monkey. I. Multimodal and discriminative properties of thermosensitive neurons. J Neurophysiol 69: 739-752, 1993.
14. Calma N. The activity of the posterior group of thalamic nuclei in the cat. J Physiol 180: 350-370, 1965.
15. Carstens E, Yokota T. Viscerosomatic convergence and responses to intestinal distension of neurons at the junction of midbrain and posterior thalamus in the cat. Exp Neurol 70: 392-402, 1980.
16. Casey KL. Unit analysis of nociceptive mechanisms in the thalamus of the awake squirrel monkey. J Neurophysiol 29: 727-750, 1966.
17. Casey KL, Minoshima S, Berger KL, Koeppe RA, Morrow TJ, Frey KA. Positron emission tomographic analysis of cerebral structures activated specifically by repetitive noxious heat stimuli. J Neurophysiol 71: 802-807, 1994.
18. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
19. Christensen BN, Perl ER. Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J Neurophysiol 33: 293-307, 1970.
20. Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, Duncan GH. Distributed processing of pain and vibration by the human brain. J Neurosci 14: 4095-4108, 1994.
21. Craig AD. Distribution of trigeminothalamic and spinothalamic lamina I terminations in the macaque monkey. J Comp Neurol 477: 119-148, 2004.
22. Craig AD. Retrograde analyses of spinothalamic projections in the Macaque monkey: input to ventral posterior nuclei. J Comp Neurol 499: 965-978, 2006.
23. Craig AD. Retrograde analyses of spinothalamic tract projections in the Macaque monkey: input to the ventral lateral nucleus. J Comp Neurol 508: 315-328, 2008.
24. Craig AD, Blomqvist A. Is there a specific lamina I spinothalamocortical pathway for pain and temperature sensations in primates? J Pain 3: 95-101, 2002.
25. Craig AD, Bushnell MC, Zhang ET, Blomqvist A. A thalamic nucleus specific for pain and temperature sensation. Nature 372: 770-773, 1994.
26. Craig AD, Krout K, Andrew D. Quantitative response characteristics of thermoreceptive and nociceptive lamina I spinothalamic neurons in the cat. J Neurophysiol 86: 1459-1480, 2001.
27. Craig AD Jr, Linington AJ, Kniffki KD. Cells of origin of spinothalamic tract projections to the medial and lateral thalamus in the cat. J Comp Neurol 289: 568-585, 1989.
28. Craig AD, Zhang E-T. Retrograde analyses of spinothalamic projections in the Macaque monkey: input to posterolateral thalamus. J Comp Neurol 499: 953-964, 2006.
29. Curry MJ. The exteroceptive properties of neurons in the somatic part of the posterior group (PO). Brain Res 44: 439-462, 1972.
30. Curry MJ, Gordon G. The spinal input to the posterior group in the cat: an electrophysiological investigation. Brain Res 44: 417-437, 1972.
31. Dado RJ, Katter JT, Giesler GJ Jr. Spinothalamic and spinohypothalamic tract neurons in the cervical enlargement of rats. I. Locations of antidromically identified axons in the thalamus and hypothalamus. J Neurophysiol 71: 959-980, 1994.
32. Davis KD, Lozano RM, Manduch M, Tasker RR, Kiss ZH, Dostrovsky JO. Thalamic relay site for cold perception in humans. J Neurophysiol 81: 1970-1973, 1999.
33. Dostrovsky JO, Craig AD. Cooling-specific spinothalamic tract neurons in the monkey. J Neurophysiol 76: 3656-3665, 1996.
34. Ferrington DG, Sorkin LS, Willis WD Jr. Responses of spinothalamic tract cells in the superficial dorsal horn of the primate lumbar spinal cord. J Physiol 388: 681-703, 1987.
35. Friedman DP, Murray EA. Thalamic connectivity of the second somatosensory area and neighboring somatosensory fields of the lateral sulcus of the Macaque. J Comp Neurol 252: 348-373, 1986.
36. Guilbaud G, Caille D, Besson JM, Benelli G. Single units activities in ventral posterior and posterior group thalamic nuclei during nociceptive and non-nociceptive stimulation in the cat. Arch Ital Bio 115: 35-56, 1977.
37. Guilbaud G, Peschanski M, Gautron M, Binder D. Neurons resonding to noxious stimulation in VB complex and caudal adjacent regions in the thalamus of the rat. Pain 8: 303-318, 1980.
38. Gauriau C, Bernard J-F. A comparative reappraisal of projections from the superficial laminae of the dorsal horn in the rat: the forebrain. J Comp Neurol 468: 24-56, 2004a.
39. Gauriau C, Bernard J-F. Posterior triangular thalamic neurons convey nociceptive messages to the secondary somatosensory and insular cortices in the rat. J Neurosci 24: 752-761, 2004b.
40. Giesler GJ Jr, Yezeirski RP, Gerhart KD, Willis WD. Spinothalamic tract neurons that project to medial and/or lateral thalamic nuclei: evidence for a physiologically novel population of spinal cord neurons. J Neurophysiol 46: 1285-1308, 1981.
41. Graziano A, Jones EG. Widespread thalamic terminations of fibers arising in the superficial medullary dorsal horn of monkeys and their relation to calbindin immunoreactivity. J Neurosci 24: 248-256, 2004.
42. Hirai T, Jones EG. A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev 14: 1-34, 1989.
43. Hylden JL, Hayashi H, Dubner R, Bennett GJ. Physiology and morphology of the lamina I spinomesenchepalic projection. J Comp Neurol 247: 505-515, 1986.
44. Jones EG. A pain in the thalamus. J Pain 3: 102-104, 2002.
45. Jones EG. The Thalamus. Cambridge, UK: Cambridge, 2007.
46. Jones EG, Burton H. Cytoarchitecture and somatic sensory connectivity of thalamic nuclei other than the ventrobasal complex in the cat. J Comp Neurol 154: 395-432, 1974.
47. Kenshalo DR Jr, Giesler GJ Jr, Leonard RB, Willis WD. Responses of neurons in the primate ventral posterior lateral nucleus to noxious stimuli. J Neurophysiol 43: 1594-1614, 1980.
48. Kenshalo DR Jr, Leonard RB, Chung JM, Willis WD. Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. J Neurophysiol 42: 1370-1389, 1979.
49. Kevetter GA, Willis WD. Collaterals of spinothalamic cells in the rat. J Comp Neurol 215: 453-464, 1983.
50. Kim JH, Greenspan JD, Coghill RC, Ohara S, Lenz FA. Lesions limited to the human thalamic principal somatosensory nucleus (ventral caudal) are associated with loss of cold sensations and central pain. J Neurosci 27: 4995-5005, 2007.
51. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184, 2000.
52. LeDoux JE, Farb C, Ruggiero DA. Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10: 1043-1054, 1990.
53. LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ. Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264: 123-146, 1987.
54. Lee JI, Dougherty PM, Antezana D, Lenz FA. Responses of neurons in the region of human thalamic principal somatic sensory nucleus to mechanical and thermal stimuli graded into the painful range. J Comp Neurol 410: 541-555, 1999.
55. Lenz FA, Dougherty PM. Neurons in the human thalamic somatosensory nucleus (Ventralis caudalis) respond to innocuous cool and mechanical stimuli. J Neurophysiol 79: 2227-2230, 1998.
56. Lenz FA, Seike M, Lin YC, Baker FH, Rowland LH, Gracely RH, Richardson RT. Neurons in the area of human thalamic nucleus ventalis caudalis respond to painful heat stimuli. Brain Res 623: 235-240, 1993a.
57. Lenz FA, Seike M, Richardson RT, Lin YC, Baker FH, Khoja I, Jaeger CJ, Gracely RH. Thermal and pain sensations evoked by microstimulation in the area of human ventrocaudal nucleus. J Neurophysiol 70: 200-212, 1993b.
58. Lipski J. Antidromic activation of neurons as an analytic tool in the study of the central nervous system. J Neurosci Methods 4: 1-32, 1981.
59. Lu G, Henderson D, Liu L, Reinhart PH, Simon SA. TRPV1b, a functional human vanilloid receptor splice variant. Mol Pharmacol 67: 1119-1127, 2005.
60. Matsumoto N, Sato T, Sawano H, Tochinai A, Suzuki TA. Characteristics of tooth pulp-driven neurons in the posterior group of the cat thalamus. Neurosci Lett 93: 253-258, 1988.
61. Mehler WR. Some neurological species differences-a posteriori. Ann NY Acad Sci 167: 424-468, 1969.
62. Mehler WR, Feferman ME, Nauta WJH. Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain 83: 718-750, 1960.
63. Montes C, Magnin M, Maarrawi J, Frot M, Convers P, Mauguiere F, Garcia-Larrea L. Thalamic thermo-algesic transmission: ventral posterior (VP) complex versus VMpo in the light of a thalamic infarct with central pain. Pain 113: 223-232, 2005.
64. Nagy I, Rang HP. Similarities and differences between the responses of rat sensory neurons to noxious heat and capsaicin. J Neurosci 19: 10647-10655, 1999.
65. Nyquist JK, Greenhoot JH. Unit analysis of nonspecific thalamic responses to high-intensity cutaneous input in the cat. Exp Neurol 42: 609-622, 1974.
66. Ohara S, Lenz FA. Medial lateral extent of thermal and pain sensations evoked by microstimulation in somatic sensory nuclei of human thalamus. J Neurophysiol 90: 2367-2377, 2003.
67. Olszewski J. The Thalamus of the Macaca mulatta: An Atlas for use with the Stereotaxic Instrument. Basel: Karger, 1952.
68. Patapoutian A, Peier AM, Story GM, Viswanath V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nat Rev Neurosci 4: 529-539, 2003.
69. Perl ER, Whitlock DG. Somatic stimuli exciting spinothalamic projections to thalamic neurons in cat and monkey. Exp Neurol 3: 256-296, 1961.
70. Poggio GF, Mountcastle VB. Study of the functional contributions of the lemniscal and spinothalamic systems to somatic sensibility. Johns Hopkins Hosp Bull 106: 266-316, 1960.
71. Price DD, Dubner R, Hu JW. Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal and, nociceptive stimulation of monkey's face. J Neurophysiol 39: 936-953, 1976.
72. Ralston HJ 3rd. Pain, the brain, and the (calbindin) stain. J Comp Neurol 459: 329-333, 2003.
73. Ralston HJ 3rd, Ralston DD. The primate dorsal spinothalamic tract: evidence for a specific termination in the posterior nuclei (Po/SG) of the thalamus. Pain 48: 107-118, 1992.
74. Ranck JB. Which elements are excited by electrical stimulation of mammalian central nervous system: a review. Brain Res. 98: 417-440, 1975.
75. Rausell E, Bae CS, Viñuela A, Huntley GW, Jones EG. Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations. J Neurosci 12: 4088-4111, 1992.
76. Ringkamp M, Peng YB, Wu G, Hartke TV, Campbell JN, Meyer RA. Capsaicin responses in heat-sensitive and heat-insensitive A-fiber nociceptors. J Neurosci 21: 4460-4468, 2001.
77. Rockel AJ, Heath CJ, Jones EG. Afferent connections to the diencephalon in the marsupial phalanger and question of sensory convergence in the "posterior group" of the thalamus. J Comp Neurol 145: 105-129, 1972.
78. Shi C, Davis M. Pain pathways involved in fear conditioning measured with fear-potentiated startle: lesion studies. J Neurosci 19: 420-430, 1999.
79. Simone DA, Zhang X, Li J, Zhang JM, Honda CN, LaMotte RH, Giesler GJ, Jr. Comparison of responses of primate spinothalamic tract neurons to pruritic and algogenic stimuli. J Neurophysiol 91: 213-222, 2004.
80. Stepniewska I, Sakai ST, Qi H-X, Kaas JH. Somatosensory input to the ventrolateral thalamic region in the macaque monkey: a potential substrate for Parkinsonian tremor. J Comp Neurol 455: 378-395, 2003.
81. Stevens RT, London SM, Apkarian AV. Spinothalamocortical projections to the secondary somatosensory cortex (SII) in squirrel monkey. Brain Res 631: 241-246, 1993.
82. Treede RD, Apkarian AV, Bromm B, Greenspan JD, Lenz FA. Cortical representation of pain: functional characterization of nociceptive areas near the lateral sulcus. Pain 87: 113-119, 2000.
83. Whitlock DG, Perl ER. Thalamic projections of spinothalamic pathways in monkey. Exp Neurol 3: 240-255, 1961.
84. Willis WD Jr, Coggeshall RE. Sensory Mechanism of the Spinal Cord. New York: Kluwer Academic/Plenum Publishers, 2004.
85. Willis WD, Trevino DL, Coulter JD, Maunz RA. Responses of primate spinothalamic tract neurons to natural stimulation of hindlimb. J Neurophysiol 37: 358-372, 1974.
86. Willis WD Jr, Zhang X, Honda CN, Giesler GJ Jr. Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus. Pain 92: 267-276, 2001.
87. Willis WD, Zhang X, Honda CN, Giesler GJ Jr. A critical review of the role of the proposed VMpo nucleus in pain. J Pain 3: 79-94, 2002.
88. Zhang X, Davidson S, Giesler GJ Jr. Thermally identified subgroups of marginal zone neurons project to distinct regions of the ventral posterior lateral nucleus in rats. J Neurosci 26: 5215-5223, 2006.
89. Zhang X, Giesler GJ Jr. Response characteristics of spinothalamic tract neurons that project to the posterior thalamus in rats. J Neurophysiol 93: 2552-2564, 2005.
90. Zhang X, Honda CN, Giesler GJ Jr. Position of spinothalamic tract axons in upper cervical spinal cord of monkeys. J Neurophysiol 84: 1180-1185, 2000b.
91. Zhang X, Wenk HN, Gokin AP, Honda CN, Giesler GJ Jr. Physiological studies of spinohypothalamic tract neurons in the lumbar enlargement of monkeys. J Neurophysiol 82: 1054-1058, 1999.
92. Zhang X, Wenk HN, Honda CN, Giesler GJ Jr. Locations of spinothalamic tract axons in cervical and thoracic spinal cord white matter in monkeys. J Neurophysiol 83: 2869-2880, 2000a.