Somatotopic activation in the human trigeminal pain pathway

Journal of Neuroscience

Volumn 22, Issue 18, 2002, Pages 8183-8192

  DaSilva, Alex F M ^a   Becerra L , Lino ^a   Makris, Nikos ^a   Strassman, Andrew M ^b   Gonzalez, R Gilberto ^a   Geatrakis, Nina ^a   Borsook, David ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Functional magnetic resonance imaging; Noxious heat; Pain; Somatosensory cortex; Somatotopy; Spinal nucleus of V; Trigeminal nucleus; Trigeminal system; Ventrobasal complex

Indexed keywords

ADULT; ARTICLE; BRAIN MAPPING; BRAIN STEM; FACE; HUMAN; HUMAN EXPERIMENT; HYPOTHALAMUS NUCLEUS; IMAGE ANALYSIS; MALE; MEDULLA OBLONGATA; NERVE CELL PLASTICITY; NERVE FIBER; NOCICEPTIVE STIMULATION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PONS; PRIORITY JOURNAL; SOMATOSENSORY CORTEX; SPINAL CORD DORSAL HORN; SPINOTHALAMIC TRACT; STIMULUS RESPONSE; THALAMUS; THERMAL STIMULATION; TRIGEMINAL NERVE; TRIGEMINAL NUCLEUS;

EID: 0037107168     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-18-08183.2002     Document Type: Article

References (76)

1. Afshar F, Dykes E (1984) Computer-generated three-dimensional visualization of the trigeminal nuclear complex. Surg Neurol 22:189-196.
2. Apkarian AV, Gelnar PA, Krauss BR, Szeverenyi NM (2000a) Cortical responses to thermal pain depend on stimulus size: A functional MRI study. J Neurophysiol 83:3113-3122.
3. Apkarian AV, Shi T, Bruggemann J, Airapetian LR (2000b) Segregation of nociceptive and non-nociceptive networks in the squirrel monkey somatosensory thalamus. J Neurophysiol 84:484-494.
4. Becerra LR, Breiter HC, Stojanovic M, Fishman S, Edwards A, Comite AR, Gonzalez RG, Borsook D (1999) Human brain activation under controlled thermal stimulation and habituation to noxious heat: An fMRI study. Magn Reson Med 41:1044-1057.
5. Becerra L, Breiter HC, Wise R, Gonzalez RG, Borsook D (2001) Reward circuitry activation by noxious thermal stimuli: Neuron 32:927-946.
6. Blomqvist A, Zhang ET, Craig AD (2000) 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.
7. Brown JA (1997) The trigeminal complex: Anatomy and physiology. Neurosurg Clin North Am 8:1-10.
8. Bushnell MC, Duncan GH, Dubner R, He LF (1984) Activity of trigeminothalamic neurons in medullary dorsal horn of awake monkeys trained in a thermal discrimination task. J Neurophysiol 52:170-187.
9. Bushnell MC, Duncan GH, Tremblay N (1993) Thalamic VPM nucleus in the behaving monkey. I. Multimodal and discriminative properties of thermosensitive neurons. J Neurophysiol 69:739-752.
10. Bushnell MC, Duncan GH, Hofbauer RK, Ha B, Chen JI, Carrier B (1999) Pain perception: Is there a role for primary somatosensory cortex? Proc Natl Acad Sci USA 96:7705-7709.
11. Carpenter MB, Sutin J (1983) Human Neuroanatomy. Baltimore: Williams & Wilkins.
12. Casey KL, Morrow TJ (1983) Ventral posterior thalamic neurons differentially responsive to noxious stimulation of the awake monkey. Science 221:675-677.
13. Casey KL, Minoshima S, Morrow TJ, Koeppe RA (1996) Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. J Neurophysiol 76:571-581.
14. Chudler EH, Anton F, Dubner R, Kenshalo Jr DR (1990) Responses of nociceptive S1 neurons in monkeys and pain sensation in humans elicited by noxious thermal stimulation: Effect of interstimulus interval. J Neurophysiol 63:559-569.
15. Chung JM, Lee KH, Surmeier DJ, Sorkin LS, Kim J, Willis WD (1986) Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J Neurophysiol 56:370-390.
16. Coghill RC, Talbot JD, Evans AC, Meyer E, Gjedde A, Bushnell MC, Duncan GH (1994) Distributed processing of pain and vibration by the human brain. J Neurosci 14:4095-4108.
17. Coghill RC, Sang CN, Maisog JM, Iadarola MJ (1999) Pain intensity processing within the human brain: A bilateral, distributed mechanism. J Neurophysiol 82:1934-1943.
18. Coghill RC, Gilron I, Iadarola MJ (2001) Hemispheric lateralization of somatosensory processing. J Neurophysiol 85:2602-2612.
19. Craig AD, Dostrovsky JO (2001) Differential projections of thermoreceptive and nociceptive lamina I trigeminothalamic and spinothalamic neurons in the cat. J Neurophysiol 86:856-870.
20. Craig AD, Zhang ET, Blomqvist A (1999) A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey. J Comp Neurol 404:221-234.
21. Dallel R, Duale C, Molat JL (1998) Morphine administered in the substantia gelatinosa of the spinal trigeminal nucleus caudalis inhibits nociceptive activities in the spinal trigeminal nucleus oralis. J Neurosci 18:3529-3536.
22. DaSilva AFM, Becerra L, Geatrakas C, Strassman A, Makris N, Keith D, Gonzalez G, Breiter H, Borsook D (2001) fMRI activation in the trigeminal pain pathways (spV, thalamus, SI) following noxious heat. Soc Neurosci Abstr 27:1328.
23. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neurolmage 9:179-194.
24. Davis KD, Kwan CL, Crawley AP, Mikulis DJ (1998) Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. J Neurophysiol 80:1533-1546.
25. Dostrovsky JO (2000) Role of thalamus in pain. Prog Brain Res 129:245-257.
26. Dostrovsky JO, Guilbaud G (1990) Nociceptive responses in medial thalamus of the normal and arthritic rat. Pain 40:93-104.
27. Dubner R, Kenshalo Jr DR, Maixner W, Bushnell MC, Oliveras JL (1989) The correlation of monkey medullary dorsal horn neuronal activity and the perceived intensity of noxious heat stimuli. J Neurophysiol 62:450-457.
28. Ellrich J, Andersen OK, Messlinger K, Arendt-Nielsen L (1999) Convergence of meningeal and facial afferents onto trigeminal brainstem neurons: An electrophysiological study in rat and man. Pain 82:229-237.
29. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 9:195-207.
30. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magn Reson Med 33: 636-647.
31. Garraghtyz PE, Florence SL, Kaas JH (1990) Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1. Brain Res 528:165-169.
32. Gelnar PA, Krauss BR, Szeverenyi NM, Apkarian AV (1998) Fingertip representation in the human somatosensory cortex: An fMRI study. NeuroImage 7:261-283.
33. Gybels JM, Sweet WH (1989) In: Neurosurgical Treatment of Persistent Pain. Basel: Karger.
34. Haines D (1994) Neuroanatomy: An Atlas of Structures, Sections, and Systems. Baltimore: Williams & Wilkins.
35. Hayashi T, Konishi S, Hasegawa I, Miyashita Y (1999) Short communication: Mapping of somatosensory cortices with functional magnetic resonance imaging in anaesthetized macaque monkeys. Eur J Neurosci 11:4451-4456.
36. Hlustik P, Solodkin A, Gullapalli RP, Noll DC, Small SL (2001) Somatotopy in human primary motor and somatosensory hand representations revisited. Cereb Cortex 11:312-321.
37. Hofbauer RK, Rainville P, Duncan GH, Bushnell MC (2001) Cortical representation of the sensory dimension of pain. J Neurophysiol 86:402-411.
38. Hsieh JC, Hannerz J, Ingvar M (1996) Right-lateralised central processing for pain of nitroglycerin-induced cluster headache. Pain 67:59-68.
39. Hu JW, Dostrovsky JO, Sessle BJ (1981) Functional properties of neurons in cat trigeminal subnucleus caudalis (medullary dorsal horn). I. Responses to oral-facial noxious and nonnoxious stimuli and projections to thalamus and subnucleus oralis. J Neurophysiol 45:173-192.
40. Jacquin MF, Rhoades RW (1990) Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens Mot Res 7:265-288.
41. Jain N, Qi HX, Catania KC, Kaas JH (2001) Anatomic correlates of the face and oral cavity representations in the somatosensory cortical area 3b of monkeys. J Comp Neurol 429:455-468.
42. Jawahar A, Kondziolka D, Kanal E, Bissonette DJ, Lunsford LD (2001) Imaging the trigeminal nerve and pons before and after surgical intervention for trigeminal neuralgia. Neurosurgery 48:101-106.
43. Kaas JH (1983) What, if anything, is SI? Organization of first somatosensory area of cortex. Physiol Rev 63:206-231.
44. Kennedy DN, Makris N, Bates JF, Caviness Jr VS (1997) Structural morphometry of the developing brain. In: Developmental Neuroimaging: Mapping the Development of Brain and Behavior (Thatcher RW, Lyon GR, Rumsey J, Krasnegor N, eds), pp 29-41. San Diego: Academic.
45. Kim JS, Lee JH, Lee MC (1997) Patterns of sensory dysfunction in lateral medullary infarction. Clinical-MRI correlation. Neurology 49:1557-1563.
46. Koyama N, Nishikawa Y, Yokota T (1998) Distribution of nociceptive neurons in the ventrobasal complex of macaque thalamus. Neurosci Res 31:39-51.
47. Kunc Z (1970) Significant factors pertaining to the results of trigeminal tractotomy. In: Trigeminal Neuralgia, Pathogenesis and Pathophysiology (Hassler R, Walker AE, eds), pp 90-100. Stuttgart: Thieme.
48. Kurth R, Villringer K, Mackert BM, Schwiemann J, Braun J, Curio G, Villringer A, Wolf KJ (1998) fMRI assessment of somatotopy in human Brodmann area 3b by electrical finger stimulation. NeuroReport 9:207-212.
49. Lenz FA, Dostrovsky JO, Tasker RR, Yamashiro K, Kwan HC, Murphy JT (1988) Single-unit analysis of the human ventral thalamic nuclear group: Somatosensory responses. J Neurophysiol 59:299-316.
50. Lin W, Kuppusamy K, Haacke EM, Burton H (1996) Functional MRI in human somatosensory cortex activated by touching textured surfaces. J Magn Reson Imaging 6:565-572.
51. Maixner W, Dubner R, Kenshalo Jr DR, Bushnell MC, Oliveras JL (1989) Responses of monkey medullary dorsal horn neurons during the detection of noxious heat stimuli. J Neurophysiol 62:437-449.
52. Manger PR, Woods TM, Jones EG (1996) Representation of face and intra-oral structures in area 3b of macaque monkey somatosensory cortex. J Comp Neurol 371:513-521.
53. May A, Kaube H, Buchel C, Eichten C, Rijntjes M, Juptner M, Weiller C, Diener HC (1998) Experimental cranial pain elicited by capsaicin: A PET study. Pain 74:61-66.
54. Merzenich MM, Kaas JH, Sur M, Lin CS (1978) Double representation of the body surface within cytoarchitectonic areas 3b and 1 in "SI" in the owl monkey (Aotus trivirgatus). J Comp Neurol 181:41-73.
55. Moore CI, Stern CE, Corkin S, Fischl B, Gray AC, Rosen BR, Dale AM (2000) Segregation of somatosensory activation in the human rolandic cortex using fMRI. J Neurophysiol 84:558-569.
56. Penfield W, Rasmussen T (1950) Secondary sensory and motor representation. In: The Cerebral Cortex of Man, pp 109-134 New York: Macmillan.
57. Peyron R, Laurent B, Garcia-Larrea L (2000) Functional imaging of brain responses to pain. A review and meta-analysis. Neurophysiol Clin 30:263-288.
58. Price DD, Dubner R, Hu JW (1976) Trigeminothalamic neurons in nucleus caudalis responsive to tactile, thermal, and nociceptive stimulation of monkey's face. J Neurophysiol 39:936-953.
59. Raboisson P, Dallel R, Clavelou P, Sessle BJ, Woda A (1995) Effects of subcutaneous formalin on the activity of trigeminal brain stem nociceptive neurones in the rat. J Neurophysiol 73:496-505.
60. Rausell E, Jones EG (1991) 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 11:226-237.
61. Ro JY, Capra NF (1999) Evidence for subnucleus interpolaris in craniofacial muscle pain mechanisms demonstrated by intramuscular injections with hypertonic saline. Brain 842:166-183.
62. Sato K, Nariai T, Sasaki S, Yazawa I, Mochida H, Miyakawa N, MomoseSato Y, Kamino K, Ohta Y, Hirakawa K, Ohno K (2002) Intraoperative intrinsic optical imaging of neuronal activity from subdivisions of the human primary somatosensory cortex. Cereb Cortex 12:269-280.
63. Servos P, Engel SA, Gati J, Menon R (1999) fMR1 evidence for an inverted face representation in human somatosensory cortex. NeuroReport 10:1393-1395.
64. Sessle BJ, Hu JW, Amano N, Zhong G (1986) Convergence of cutaneous, tooth pulp, visceral, neck and muscle afferents onto nociceptive and non-nociceptive neurones in trigeminal subnucleus caudalis (medullary dorsal horn) and its implications for referred pain. Pain 27:219-235.
65. Sherman SE, Luo L, Dostrovsky JO (1997) Spinal strychnine alters response properties of nociceptive-specific neurons in rat medial thalamus. J Neurophysiol 78:628-637.
66. Strassman AM, Vos BP (1993) Somatotopic and laminar organization of fos-like immunoreactivity in the medullary and upper cervical dorsal horn induced by noxious facial stimulation in the rat. J Comp Neurol 331:495-516.
67. Strassman AM, Mineta Y, Vos BP (1994) Distribution of fos-like immunoreactivity in the medullary and upper cervical dorsal horn produced by stimulation of dural blood vessels in the rat. J Neurosci 14:3725-3735.
68. Svensson P, Minoshima S, Beydoun A, Morrow TJ, Casey KL (1997) Cerebral processing of acute skin and muscle pain in humans. J Neurophysiol 78:450-460.
69. Talairach J, Tournoux P (1988) Co-Planar Stereotaxic Atlas of the Human Brain. Stuttgart: Thieme.
70. Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH (1991) Multiple representations of pain in human cerebral cortex. Science 251:1355-1358.
71. Usunoff KG, Marani E, Schoen JH (1997) The trigeminal system in man. Adv Anat Embryol Cell Biol 136:1-126.
72. Weiller C, May A, Limmroth V, Juptner M, Kaube H, Schayck RV, Coenen HH, Diener HC (1995) Brain stem activation in spontaneous human migraine attacks. Nat Med 1:658-660.
73. Williams MN, Zahm DS, Jacquin MF (1994) Differential foci and synaptic organization of the principal and spinal trigeminal projections to the thalamus in the rat. Eur J Neurosci 6:429-453.
74. Yokota T, Koyama N, Matsumoto N (1985) Somatotopic distribution of trigeminal nociceptive neurons in ventrobasal complex of cat thalamus. J Neurophysiol 53:1387-1400.
75. Young RF, Perryman KM (1986) Neuronal responses in rostral trigeminal brain-stem nuclei of macaque monkeys after chronic trigeminal tractotomy. J Neurosurg 65:508-516.
76. Zubieta JK, Smith YR, Bueller JA, Xu Y, Kilbourn MR, Jewett DM, Meyer CR, Koeppe RA, Stohler CS (2001) Regional μ opioid receptor regulation of sensory and affective dimensions of pain. Science 293:311-315.