Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the posterior portion of the ventral medial nucleus, in the human thalamus

Brain

Volumn 123, Issue 3, 2000, Pages 601-619

  Blomqvist, Anders ^a   Zhang, En Tan ^b   Craig, A D ^b  

^a LINKÖPING UNIVERSITY   (Sweden)

^b NONE

Author keywords

Calbindin; Calcitonin gene related peptide; Posterior complex; Spinothalamic tract; Substance P

Indexed keywords

CALBINDIN; CALCITONIN GENE RELATED PEPTIDE; SUBSTANCE P;

ADULT; AGED; ANALGESIA; ARTICLE; BRAIN INFARCTION; CELL AGGREGATION; CELL SHAPE; CYTOARCHITECTURE; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MEDIAL GENICULATE BODY; NERVE ENDING; NERVE FIBER; NOCICEPTION; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; PULVINAR; SENSORY NERVE; SPINOTHALAMIC TRACT; TEMPERATURE SENSE; THALAMUS PARAFASCICULAR NUCLEUS; THALAMUS VENTRAL NUCLEUS; THERMORECEPTOR;

EID: 0033969885     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/123.3.601     Document Type: Article

References (108)

1. Apkarian AV, Hodge CJ. A dorsolateral spinothalamic tract in macaque monkey. Pain 1989; 37: 323-33.
2. Apkarian AV, Shi T. Squirrel monkey lateral thalamus. I. Somatic nociresponsive neurons and their relation to spinothalamic terminals. J Neurosci 1994; 14: 6779-95.
3. Apkarian AV, Stevens RT, Hodge CJ. Funicular location of ascending axons of lamina I cells in the cat spinal cord. Brain Res 1985; 334: 160-4.
4. Arvidsson U, Cullheim S, Ulfhake B, Hökfelt T, Terenius L. Altered levels of calcitonin gene-related peptide (CGRP)-like immunoreactivity of cat lumbar motoneurons after chronic spinal cord transection. Brain Res 1989; 489: 387-91.
5. Battaglia G, Rustioni A. Substance P innervation of the rat and cat thalamus. II. Cells of origin in the spinal cord. J Comp Neurol 1992; 315: 473-86.
6. Battaglia G, Spreafico R, Rustioni A. Substance P-immunoreactive fibres in the thalamus from ascending somatosensory pathways. In: Bentivoglio M, Spreafico R, editors. Cellular thalamic mechanisms. Amsterdam: Excerpta Medica; 1988. p. 365-74.
7. Beckstead RM, Morse JR, Norgren R. The nucleus of the solitary tract in the monkey: projections to the thalamus and brain stem nuclei. J Comp Neurol 1980; 190: 259-82.
8. Berkley KJ. Spatial relationships between the terminations of somatic sensory and motor pathways in the rostral brainstem of cats and monkeys. I. Ascending somatic sensory inputs to lateral diencephalon. J Comp Neurol 1980; 193: 283-317.
9. Berthier M, Starkstein S, Leiguarda R. Asymbolia for pain: a sensory-limbic disconnection syndrome. Ann Neurol 1988; 24: 41-9.
10. Bettag W, Yoshida T. Über stereotaktischen Schmerzoperationen. Acta Neurochir (Wien) 1960; 8: 299-317.
11. Biemond A. The conduction of pain above the level of the thalamus opticus. Arch Neurol Psychiat 1956; 75: 231-44.
12. Bishop GH. The relation between nerve fiber size and sensory modality: phylogenetic implications of the afferent innervation of cortex. J Nerv Ment Dis 1959; 128: 89-114.
13. Blomqvist A, Mackerlova L. Spinal projections to the parabrachial nucleus are substance P-immunoreactive. Neuroreport 1995; 6: 605-8.
14. Blomqvist A, Ericson A-C, Craig AD, Broman J. Evidence for glutamate as a neurotransmitter in spinothalamic tract terminals in the posterior region of owl monkeys. Exp Brain Res 1996; 108: 33-44.
15. Blomqvist A, Zhang E-T, Craig AD. Immunohistochemical characterization of the VMpo in the human thalamus [abstract]. Soc Neurosci Abstr 1998; 24: 1129.
16. Bogousslavsky J, Regli F, Uske A. Thalamic infarcts: clinical syndromes, etiology, and prognosis. Neurology 1988; 38: 837-48.
17. Boivie J. An anatomical reinvestigation of the termination of the spinothalamic tract in the monkey. J Comp Neurol 1979; 186: 343-69.
18. Boivie J, Leijon G. Clinical findings in patients with central poststroke pain. In: Casey KL, editor. Pain and central nervous system disease: the central pain syndromes. New York: Raven Press, 1991. p. 65-122.
19. Bowsher D. Termination of the central pain pathway in man: the conscious appreciation of pain. Brain 1957; 80: 606-22.
20. Bowsher D, Leijon G, Thuomas KA. Central poststroke pain: correlation of MRI with clinical pain characteristics and sensory abnormalities. Neurology 1998; 51: 1352-8.
21. Burton H, Craig AD. Spinothalamic projections in cat, raccoon and monkey: a study based on anterograde transport of horseradish peroxidase. In: Macchi G, Rustioni A, Spreafico R, editors. Somatosensory integration in the thalamus. Amsterdam: Elsevier; 1983. p. 17-41.
22. Bushnell MC, Duncan GH, Tremblay N. Thalamic VPM nucleus in the behaving monkey. 1. Multimodal and discriminative properties of thermosensitive neurons. J Neurophysiol 1993; 69: 739-752.
23. 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 1994; 71: 802-7.
24. Cechetto DF, Saper CB. Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 1987; 262: 27-45.
25. Christensen BN, Perl ER. Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. J Neurophysiol 1970; 33: 293-307.
26. Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, et al. Distributed processing of pain and vibration by the human brain. J Neurosci 1994; 14: 4095-108.
27. Craig AD. Spinal distribution of ascending lamina I axons anterogradely labeled with Phaseolus vulgaris leucoagglutinin (PHA-L) in the cat. J Comp Neurol 1991; 313: 377-93.
28. Craig AD. Supraspinal projections of lamina I neurons. In: Besson JM, Guilbaud G, Ollat H, editors. Forebrain areas involved in pain processing. Paris: John Libbey Eurotext; 1995. p. 13-25.
29. Craig AD. An ascending general homeostatic afferent pathway originating in lamina I. In: Holstege G, Bandler R, Saper CB, editors. The emotional motor system. Progress in brain research. Vol. 107. Amsterdam: Elsevier; 1996a. p. 225-42.
30. Craig AD. Pain, temperature, and the sense of the body. In: Franzen O, Johansson R, Terenius L, editors. Somesthesis and the neurobiology of the somatosensory cortex. Basel: Birkhäuser; 1996b. p. 27-39.
31. Craig AD. A new version of the thalamic disinhibition hypothesis of central pain. Pain Forum 1998; 7: 1-14.
32. Craig AD, Bushnell MC. The thermal grill illusion: unmasking the burn of cold pain. Science 1994; 265: 252-5.
33. Craig AD, Dostrovsky JO. Medulla to thalamus. In: Wall PD, Melzack R, editors. Textbook of pain. 4th ed. Edinburgh: Churchill Livingstone; 1999. p. 183-214.
34. Craig AD, Kniffki K-D. Spinothalamic lumbosacral lamina I cells responsive to skin and muscle stimulation in the cat. J Physiol (Lond) 1985; 365: 197-221.
35. Craig AD, Serrano LP. Effects of systemic morphine on lamina I spinothalamic tract neurons in the cat. Brain Res 1994; 636: 233-44.
36. Craig AD, Zhang E-T. Anterior cingulate projection from MDvc (a lamina I spinothalamic target in the medial thalamus of the monkey) [abstract]. Soc Neurosci Abstr 1996; 22: 111.
37. Craig AD, Bushnell MC, Zhang E-T, Blomqvist A. A thalamic nucleus specific for pain and temperature sensation. Nature 1994; 372: 770-3.
38. Craig AD, Reiman EM, Evans A, Bushnell MC. Functional imaging of an illusion of pain. Nature 1996; 384: 258-60.
39. Craig AD, Zhang E-T, Blomqvist A. Immunohistochemical identification of ascending lamina I axons in the lateral spinothalamic tract [abstract]. Soc Neurosci Abstr 1998; 24: 387.
40. Craig AD, Zhang E-T, Blomqvist A. A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey. J Comp Neurol 1999; 404: 221-34.
41. Davis KD, Tasker RD, Kiss ZH, Hutchison WD, Dostrovsky JO. Visceral pain evoked by thalamic microstimulation in humans. Neuroreport 1995; 6: 369-74.
42. Davis KD, Kiss, ZH, Tasker RR, Dostrovsky JO. Thalamic stimulation-evoked sensations in chronic pain patients and in nonpain (movement disorder) patients. J Neurophysiol 1996; 75: 1026-37.
43. Davis KD, Lozano AM, Manduch M, Tasker RR, Kiss ZHT, Dostrovsky JO. Thalamic relay site for cold perception in humans. J Neurophysiol 1999; 81: 1970-3.
44. Davison C, Schick W. Spontaneous pain and other subjective sensory disturbances. Arch Neurol Psychiat 1935; 34: 1204-37.
45. Dostrovsky JO, Craig AD. Cooling-specific spinothalamic neurons in the monkey. J Neurophysiol 1996a; 76: 3656-65.
46. Dostrovsky JO, Craig AD. Nociceptive neurons in primate insular cortex [abstract]. Soc Neurosci Abstr 1996b; 22: 111.
47. Dostrovsky JO, Davis KD, Kiss ZHT, Junn F, Lozano AM. Evidence for a specific temperature relay site in human thalamus. In: 8th World Congress on Pain; IASP Press; 1996. p. 440.
48. 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 1986; 252: 348-73.
49. Fulwiler CE, Saper CB. Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 1984; 319: 229-59.
50. Greenspan JD, Winfield JA. Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum. Pain 1992; 50: 29-39.
51. Halsell CB, Travers SP. Anterior and posterior oral cavity responsive neurons are differentially distributed among parabrachial subnuclei in rat. J Neurophysiol 1997; 78: 920-38.
52. Han Z-S, Zhang E-T, Craig AD. Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nat Neurosci 1998; 1: 218-25.
53. Hassler E. Achitectonic organization of the thalamic nuclei. In: Schaldenbrand G, Walker AE, editors. Stereotaxy of the human brain. Stuttgart: Thieme; 1982. p. 92-112.
54. Hassler R, Riechert T. Klinische und anatomische Befunde bei stereotaktischen Schmertzoperationen im Thalamus. Arch Psychiat Nervkrankh 1959; 200: 93-122.
55. Head H, Holmes G. Sensory disturbances from cerebral lesions. Brain 1911; 34: 102-254.
56. Hermanson O, Blomqvist A. Subnuclear localization of FOS-like immunoreactivity in the rat parabrachial nucleus after nociceptive stimulation. J Comp Neurol 1996; 368: 45-56.
57. Hirai T, Jones EG. Distribution of tachykinin- and enkephalin-immunoreactive fibers in the human thalamus. Brain Res Brain Res Rev 1989a; 14: 35-52.
58. Hirai T, Jones EG. A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev 1989b; 14: 1-34.
59. Hsieh JC, Hägermark M, Ståhle-Bäckdahl K, Ericson K, Eriksson L, Stone-Elander S, et al. Urge to scratch represented in the human cerebral cortex during itch. J Neurophysiol 1994; 72: 3004-8.
60. Hsu SM, Raine L, Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 1981; 29: 577-80.
61. Iwata K, Kenshalo DR Jr, Dubner R, Nahin RL. Diencephalic projections from the superficial and deep laminae of the medullary dorsal horn in the rat. J Comp Neurol 1992; 321: 404-20.
62. Jones EG. A description of the human thalamus. In: Steriade M, Jones EG, McCormick DA, editors. Thalamus, Vol. II. Experimental and clinical aspects. Amsterdam: Elsevier; 1997. p. 425-99.
63. Jones EG. Viewpoint: the core and matrix of thalamic organization. [Review], Neuroscience 1998; 85: 331-45.
64. Jones AK, Brown WD, Friston KJ, Qi LY, Frackowiak RS. Cortical and subcortical localization of response to pain in man using positron emission tomography. Proc R Soc Lond B Biol Sci 1991; 244: 39-44.
65. Karimnamazi H, Travers JB. Differential projections from gustatory responsive regions of the parabrachial nucleus to the medulla and forebrain. Brain Res 1998; 813: 283-302.
66. Kenshalo DR Jr, Giesler GJ Jr, Leonard RB, Willis WD. Responses of neurons in primate ventral posterior lateral nucleus to noxious stimuli. J Neurophysiol 1980 43: 1594-614.
67. Kruger L, Mantyh PW. Central nervous system gustatory pathways. In: Björklund A, Hökfelt T, Swanson LW, editors. Handbook of chemical neuroanatomy, Vol. 7. Integrated systems of the CNS, Part II. Central visual, auditory, somatosensory, gustatory. Amsterdam: Elsevier; 1989. p. 360-411.
68. Kruger L, Mantyh PW, Sternini C, Brecha NC, Mantyh CR. Calcitonin gene-related peptide (CGRP) in the rat central nervous system: patterns of immunoreactivity and receptor binding sites. Brain Res 1988a; 463: 223-44.
69. Kruger L, Sternini C, Brecha NC, Mantyh PW. Distribution of calcitonin gene-related peptide immunoreactivity in relation to the rat central somatosensory projection. J Comp Neurol 1988b; 273: 149-62.
70. Kruger L, Sternini C, Brecha NC, Mantyh PW. The thalamic region of calcitonin gene-related peptide (CGRP) immunoreactivity and its relation to somatosensory pathways. In: Bentivoglio M, Spreafico R, editors. Cellular thalamic mechanisms. Amsterdam: Excerpta Medica; 1988c. p. 375-86.
71. Kuru M. The sensory paths in the spinal cord and brain stem of man. Tokyo: Sogensya; 1949.
72. Leijon G, Boivie J, Johansson I. Central post-stroke pain -neurological symptoms and pain characteristics. Pain 1989; 36: 13-25.
73. Lenz FA, Seike M, Lin YC, Baker FH, Rowland LH, Gracely RH, et al. Neurons in the area of human thalamic nucleus ventralis caudalis respond to painful heat stimuli. Brain Res 1993a; 623: 235-40.
74. Lenz FA, Seike M, Richardson RT, Lin YC, Baker FH, Khoja I, et al. Thermal and pain sensations evoked by microstimulation in the area of human ventrocaudal nucleus. J Neurophysiol 1993b; 70: 200-12.
75. Lenz FA, Gracely RH, Hope EJ, Baker FH, Rowland LH, Dougherty PM, et al. The sensation of angina can be evoked by stimulation of the human thalamus. Pain 1994; 59: 119-25.
76. Lenz FA, Gracely RH, Zirh TA, Leopold DA, Rowland LH, Dougherty PM. Human thalamic nucleus mediating taste and multiple other sensations related to ingestive behavior. J Neurophysiol 1997; 77: 3406-9.
77. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, et al. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 1997; 278: 275-9.
78. Mark VH, Ervin FR, Hackett TP. Clinical aspects of stereotactic thalamotomy in the human. Arch Neurol 1960; 3: 351-67.
79. Mark VH, Ervin FR, Yakovlev PI. Stereotactic thalamotomy. III. The verification of anatomical lesion sites in the human thalamus. Arch Neurol 1963; 8: 528-38.
80. Masson C, Koskas P, Cambier J, Masson M. Left pseudothalamic cortical syndrome and pain asymbolia. [Review]. [French]. Rev Neurol (Paris) 1991; 147: 668-70.
81. May WP. The afferent path. Brain 1906; 29: 742-803.
82. Mehler WR. The posterior thalamic region in man. Confin Neurol 1966; 27: 18-29.
83. Mehler WR, Feferman ME, Nauta WJH. Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain 1960; 83: 718-50.
84. Morel A, Magnin M, Jeanmonod D. Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 1997; 387: 588-630.
85. Nathan PW, Smith MC. Clinico-anatomical correlation in anterolateral cordotomy. In: Bonica JJ, editor. Advances in pain research and therapy, Vol. 3. New York: Raven Press; 1979. p. 921-6.
86. Noguchi K, Dubner R, Ruda MA. Preproenkephalin mRNA in spinal dorsal horn neurons is induced by peripheral inflammation and is co-localized with fos and fos-related proteins. Neuroscience 1992; 46: 561-70.
87. Norgren R, Leonard CM. Taste pathways in rat brainstem. Science 1971; 173: 1136-9.
88. Norrsell U. Thermosensory defects after cervical spinal cord lesions in the cat. Exp Brain Res 1979; 35: 479-94.
89. Opdam R, Kemali M, Nieuwenhuys R. Topological analysis of the brain stem of the frogs Rana esculenta and Rana catesbeiana. J Comp Neurol 1976; 165: 307-32.
90. Pagni CA. Central pain. A neurosurgical challenge. Torino: Edizioni Minerva Medica; 1998.
91. Perl ER. Pain and nociception. In: Brookhart JM, Mountcastle VB, editors. Handbook of physiology, Sect. 1, Vol. III, Pt. 2. Bethesda: American Physiological Society; 1984. p. 915-75.
92. Pritchard TC, Hamilton RB, Norgren R. Neural coding of gustatory information in the thalamus of Macaca mulatta. J Neurophysiol 1989; 61: 1-14.
93. Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997; 277: 968-71.
94. Ralston HJ 3d, Ralston DD. The primate dorsal spinothalamic tract: evidence for a specific termination in the posterior nuclei (Po/SG) of the thalamus. Pain 1992; 48: 107-18.
95. Rausell E, Jones EG. Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex. J Neurosci 1991a; 11: 226-37.
96. Rausell E, Jones EG. Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map. J Neurosci 1991b; 11: 210-25.
97. 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 1992; 12: 4088-111.
98. Sano K. Intralaminar thalamotomy (thalamolaminotomy) and posteromedial hypothalamotomy in the treatment of intractable pain. In: Krayenbühl H, Maspes PE, Sweet WH, editors. Progress in neurological surgery. Pain - its neurosurgical management. Part II: central procedures. Basel: Karger; 1977. p. 50-103.
99. Schmahmann JD, Leifer D. Parietal pseudothalamic pain syndrome. Clinical features and anatomic correlates. Arch Neurol 1992; 49: 1032-7.
100. Sternberger LA. Immunocytochemistry. 2nd ed. New York: Wiley; 1979.
101. Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH. Multiple representations of pain in human cerebral cortex. Science 1991; 251: 1355-8.
102. Vallbo AB, Olausson H, Wessberg J. Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. J Neurophysiol 1999; 81: 2753-63.
103. Veening JG, Coolen LM. Neural activation following sexual behavior in the male and female rat brain. Behav Brain Res 1998; 92: 181-93.
104. Yamamoto T, Shimura T, Sakai N, Ozaki N. Representation of hedonics and quality of taste stimuli in the parabrachial nucleus of the rat. Physiol Behav 1994; 56: 1197-202.
105. Yasui Y, Saper CB, Cechetto DF. Calcitonin gene-related peptide immunoreactivity in the visceral sensory cortex, thalamus, and related pathways in the rat. J Comp Neurol 1989; 290: 487-501.
106. Yu XH, Zhang E-T, Craig AD, Shigemoto R, Ribeiro-da-Silva A, De Koninck Y. NK-1 receptor immunoreactivity in distinct morphological types of lamina I neurons of the primate spinal cord. J Neurosci 1999; 19: 3545-55.
107. Zhang E-T, Craig AD. Morphology and distribution of spinothalamic lamina I neurons in the monkey. J Neurosci 1997a; 17: 3274-84.
108. Zhang E-T, Craig AD. Calbindin-positive lamina I STT neurons in monkey [abstract]. Soc Neurosci Abstr 1997b; 23: 1804.