Lesions limited to the human thalamic principal somatosensory nucleus (ventral caudal) are associated with loss of cold sensations and central pain

Journal of Neuroscience

Volumn 27, Issue 18, 2007, Pages 4995-5005

  Kim, Jong H ^a   Greenspan, Joel D ^b   Coghill, Robert C ^c   Ohara, Shinji ^d   Lenz, Frederick A ^a  

^a JOHNS HOPKINS HOSPITAL   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d Kyoto Kizugawa Hospital   (Japan)

Author keywords

Cold; Human; Pain; Somatosensory; Stroke; Ventral posterior thalamus

Indexed keywords

ADULT; AGED; ARTICLE; CASE REPORT; CLINICAL FEATURE; COLD SENSITIVITY; DIAGNOSTIC PROCEDURE; DYSESTHESIA; HUMAN; IMAGING SYSTEM; MALE; NEUROPATHIC PAIN; PRIORITY JOURNAL; SENSORY DYSFUNCTION; SOMATOSENSORY CORTEX;

AGED; CEREBROVASCULAR ACCIDENT; COLD; HUMANS; MALE; MIDDLE AGED; PAIN; PAIN MEASUREMENT; TEMPERATURE SENSE; VENTRAL THALAMIC NUCLEI;

EID: 34247882866     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0716-07.2007     Document Type: Article

References (83)

1. Andersen P, Vestergaard K, Ingeman-Nielsen M, Jensen TS (1995) Incidence of post-stroke central pain. Pain 61:187-193.
2. Apkarian AV, Hodge CJ (1989) Primate spinothalamic pathways. III. Thalamic terminations of the dorsolateral and ventral spinothalamic pathways. J Comp Neurol 288:493-511.
3. Apkarian AV, Shi T, Bruggemann J, Airapetian LR (2000) Segregation of nociceptive and non-nociceptive networks in the squirrel monkey somatosensory thalamus. J Neurophysiol 84:484-494.
4. Beric A, Dimitrijevic MR, Lindblom U (1988) Central dysesthesia syndrome in spinal cord injury patients. Pain 34:109-116.
5. 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.
6. Boivie J (1999) Central pain. In: Textbook of pain (Wall PD, Melzack R, eds), pp 879-914. Edinburgh: Churchill Livingstone.
7. Boivie J, Leijon G (1991) Clinical findings in patients with central poststroke pain. In: Pain and central nervous system disease (Casey KL, ed), pp 65-75. New York: Raven.
8. Boivie J, Leijon G, Johansson I (1989) Central post-stroke pain-a study of the mechanisms through analyses of the sensory abnormalities. Pain 37:173-185.
9. Bowsher D (1996) Central pain: clinical and physiological characteristics. J Neurol Neurosurg Psychiatry 61:62-69.
10. Bowsher D, Leijon G, Thuomas KA (1998) Central poststroke pain: correlation of MRI with clinical pain characteristics and sensory abnormalities. Neurology 51:1352-1358.
11. Brown JA, Barbaro NM (2003) Motor cortex stimulation for central and neuropathic pain: current status. Pain 104:431-435.
12. Bushnell MC, Taylor MB, Duncan GH, Dubner R (1983) Discrimination of innocuous and noxious thermal stimuli applied to the face in human and monkey. Somatosens Res 1:119-129.
13. Casey KL (1991) Pain and central nervous system disease: a summary and overview. In: Pain and central nervous system disease: the central pain syndromes (Casey KL, ed), pp 1-11. New York: Raven.
14. 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.
15. Cassinari V, Pagni CA (1969) Central pain. A neurosurgical survey. Cambridge, MA: Harvard UP.
16. Cesaro P, Mann MW, Moretti JL, Defer G, Roualdes B, Nguyen JP, Degos JD (1991) Central pain and thalamic hyperactivity: a single photon emission computerized tomographic study. Pain 47:329-336.
17. Chmielowska J, Coghill RC, Maisog JM, Carson RE, Herscovitch P, Honda M, Chen R, Hallett M (1998) Positron emission tomography [15O]water studies with short interscan interval for single-subject and group analysis: influence of background subtraction. J Cereb Blood Flow Metab 18:433-443.
18. Chmielowska J, Coghill RC, Carson RE, Ishii K, chen R, Hallett M, Herscovitch P (1999) Comparison of PET [Oxygen15]water studies with 6 min and 10 min interscan intervals: single subject and group analyses. J Cereb Blood Flow Metab 19:570-582.
19. Collins DL, Neelin P, Peter TM, Evans AC (1993) Automatic 3D intersubject registration of MR volumetric data in standardized talairach space. J Comput Assist Tomogr 18:192-205.
20. Craig AD (2000) The functional anatomy of lamina I and its role in poststroke central pain. In: Nervous system plasticity and chronic pain (Sandkühler J, Bromm B, Gebhart GF, eds), pp 137-151. Amsterdam: Elsevier.
21. Craig AD (2004) Distribution of trigeminothalamic and spinothalamic lamina I terminations in the macaque monkey. J Comp Neurol 477:119-148.
22. Craig AD, Reiman EM, Evans A, Bushnell MC (1996) Functional imaging of an illusion of pain. Nature 384:258-260.
23. Davis KD (2000) Studies of pain using functional magnetic resonance im-aging. In: Pain imaging (Casey KL, Bushnell MC, eds), pp 195-210. Seattle: IASP.
24. Davis KD, Kiss ZHT, Tasker RR, Dostrovsky JO (1996) Thalamic stimulation-evoked sensations in chronic pain patients and nonpain (movement disorder) patients. J Neurophysiol 75:1026-1037.
25. 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.
26. Davis KD, Lozano RM, Manduch M, Tasker RR, Kiss ZH, Dostrovsky JO (1999) Thalamic relay site for cold perception in humans. J Neurophysiol 81:1970-1973.
27. Davis KD, Taub E, Duffner F, Lozano AM, Tasker RR, Houle S, Dostrovsky JO (2000) Activation of the anterior cingulate cortex by thalamic stimulation in patients with chronic pain: a positron emission tomography study. J Neurosurg 92:64-69.
28. Dougherty PM, Sluka KA, Sorkin LS, Westlund KN, Willis WD (1992) 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 17:1-13.
29. Duncan GH, Bushnell MC, Oliveras JL, Bastrash N, Tremblay N (1993) Thalamic VPM nucleus in the behaving monkey. III. Effects of reversible inactivation by lidocaine on thermal and mechanical discrimination. J Neurophysiol 70:2086-2096.
30. Erdem A, Yasargil MG, Roth P (1993) Microsurgical anatomy of the hippocampal arteries. J Neurosurg 79:256-265.
31. Essick GK (1992) Comprehensive clinical evaluation of perioral sensory function. Oral Maxillofac Surg Clin North Am 4:503-526.
32. Foreman RD, Kenshalo DR, Schmidt RF, Willis WD (1979) Field potentials and excitation of primate spinothalamic neurons in response to volleys in muscle afferents. J Physiol (Lond) 286:197-213.
33. 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.
34. Friston KJ, Worsley KJ, Frackowiak RSJ, Mazziotta JC, Evans AC (1994) Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp 1:210-220.
35. Graziano A, Jones EG (2004) 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.
36. Greenspan JD, Ohara S, Sarlani E, Lenz FA (2004) Allodynia in patients with post-stroke central pain (CPSP) studied by statistical quantitative sensory testing within individuals. Pain 109:357-366.
37. Gross RE, Jones EG, Dostrovsky JO, Bergeron C, Lang AE, Lozano AM (2004) Histological analysis of the location of effective thalamic stimulation for tremor. Case report. J Neurosurg 100:547-552.
38. Hillis AE, Lenz FA, Zirh TA, Dougherty PM, Eckel TS, Jackson K (1998) Hemispatial somatosensory and motor extinction after stereotactic thalamic lesions. Neurocase 4:21-34.
39. Hirai T, Jones EG (1989) A new parcellation of the human thalamus on the basis of histochemical staining. Brain Res Brain Res Rev 14:1-34.
40. Hirato M, Watanabe K, Takahashi A, Hayase N, Horikoshi S, Shibasaki T, Ohye C (1994) Pathophysiology of central (thalamic) pain: combined change of sensory thalamus with cerebral cortex around central sulcus. Stereotact Funct Neurosurg 62:300-303.
41. Jones EG (1985) The thalamus. New York: Plenum.
42. Jones EG, Friedman DP, Hendry SH (1982) Thalamic basis of place- and modality-specific columns in monkey somatosensory cortex: a correlative anatomical and physiological study. J Neurophysiol 48:545-568.
43. Katayama Y, Tsubokawa T, Yamamoto T (1994) Chronic motor cortex stimulation for central deafferentation pain: experience with bulbar pain secondary to Wallenberg syndrome. Stereotact Funct Neurosurg 62:295-299.
44. Kertesz A, Black SE, Tokar G, Benke T, Carr T, Nicholson L (1988) Periventricular and subcortical hyperintensities on magnetic resonance imaging. 'Rims, caps, and unidentified bright objects'. Arch Neurol 45:404-408.
45. Krayenbuhl H, Yasargil MG (1972) Radiological anatomy and topography of cerebral arteries. In: Handbook of clinical neurology (Vinken PJ, Bruyn GW, eds), pp 65-100. New York: Elsevier.
46. Lee J, Dougherty PM, Antezana D, Lenz FA (1999) 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.
47. Leijon G, Boivie J, Johansson I (1989) Central post-stroke painneurological symptoms and pain characteristics. Pain 36:13-25.
48. Lenz FA, Dostrovsky JO, Tasker RR, Yamashiro K, Kwan HC, Murphy JT (1988a) Single-unit analysis of the human ventral thalamic nuclear group: somatosensory responses. J Neurophysiol 59:299-316.
49. Lenz FA, Dostrovsky JO, Kwan HC, Tasker RR, Yamashiro K, Murphy JT (1988b) Methods for microstimulation and recording of single neurons and evoked potentials in the human central nervous system. J Neurosurg 68:630-634.
50. Lenz FA, Seike M, Richardson RT, Lin YC, Baker FH, Khoja I, Jaeger CJ, Gracely RH (1993a) Thermal and pain sensations evoked by microstimulation in the area of human ventrocaudal nucleus. J Neurophysiol 70:200-212.
51. Lenz FA, Seike M, Lin YC, Baker FH, Rowland LH, Gracely RH, Richardson RT (1993b) Neurons in the area of human thalamic nucleus ventralis caudalis respond to painful heat stimuli. Brain Res 623:235-240.
52. Lenz FA, Kwan HC, Martin R, Tasker R, Richardson RT, Dostrovsky JO (1994) Characteristics of somatotopic organization and spontaneous neuronal activity in the region of the thalamic principal sensory nucleus in patients with spinal cord transection. J Neurophysiol 72:1570-1587.
53. Lenz FA, Gracely RH, Baker FH, Richardson RT, Dougherty PM (1998) Reorganization of sensory modalities evoked by microstimulation in region of the thalamic principal sensory nucleus in patients with pain due to nervous system injury. J Comp Neurol 399:125-138.
54. Lenz FA, Ohara S, Gracely RH, Dougherty PM, Patel SH (2004) Pain encoding in the human forebrain: binary and analog exteroceptive channels. J Neurosci 24:6540-6544.
55. Mehler WR (1962) The anatomy of the so-called "pain tract" in man: an analysis of the course and distribution of the ascending fibers of the fasciculus anterolateralis. In: Basic research in paraplegia (French JD, Porter RW, eds), pp 26-55. Springfield, IL: Thomas.
56. Mehler WR, Feferman ME, Nauta WHJ (1960) Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain 83:718-750.
57. Montes C, Magnin M, Maarrawi J, Frot M, Convers P, Mauguiere F, Garcia-Larrea L (2005) Thalamic thermo-algesic transmission: ventral posterior (VP) complex versus VMpo in the light of a thalamic infarct with central pain. Pain 113:223-232.
58. Mountcastle VB (1984) Central nervous mechanisms in mechanoreceptive sensibility. In: Handbook of physiology, Sensory processes (Brookhart JM, Mountcastle VB, Smith ID, Geiger SR, eds), pp 789. Bethesda, MD: American Physiological Society.
59. Nathan PW, Smith MC (1996) Some tracts of the anterior and lateral columns of the spinal cord. In: Pain (Knighton RS, Dumke PR, eds), pp 47-58. Philadelphia: Lippincott, Williams, and Wilkins.
60. Nathan PW, Smith MC, Cook AW (1986) Sensory effects in man of lesions of the posterior columns and of some other afferent pathways. Brain 109:1003-1041.
61. Nguyen JP, Lefaucher JP, Le Guerinel C, Eizenbaum JF, Nakano N, Carpentier A, Brugieres P, Pollin B, Rostaing S, Keravel Y (2000) Motor cortex stimulation in the treatment of central and neuropathic pain. Arch Med Res 31:263-265.
62. Noordenbos W, Wall PD (1976) Diverse sensory functions with an almost totally divided spinal cord. A case of spinal cord transection with preservation of part of one anterolateral quadrant. Pain 2:185-195.
63. Nowinski W, Bryan RN, Raghavan R (1996) The electronic clinical brain atlas. New York: Thieme.
64. Ohara S, Lenz FA (2003) Medial lateral extent of thermal and pain sensations evoked by microstimulation in somatic sensory nuclei of human thalamus. J Neurophysiol 90:2367-2377.
65. Ohara S, Weiss N, Lenz FA (2004) Microstimulation in the region of the human thalamic principal somatic sensory nucleus evokes sensations like those of mechanical stimulation and movement. J Neurophysiol 91:736-745.
66. Patel S, Ohara S, Dougherty PM, Gracely RH, Lenz FA (2006) Psychophysical elements of place and modality specificity in the thalamic somatic sensory nucleus (ventral caudal, vc) of awake humans. J Neurophysiol 95:646-659.
67. Peyron R, Garcia-Larrea L, Gregoire MC, Convers P, Lavenne F, Veyre L, Froment JC, Mauguiere F, Michel D, Laurent B (1998) Allodynia after lateral-medullary (Wallenberg) infarct: a PET study. Brain 121:345-356.
68. Price DD, Bush FM, Long S, Harkins SW (1994) A comparison of pain measurement characteristics of mechanical visual analogue and simple numerical rating scales. Pain 56:217-226.
69. Rainville P, Bushnell MC, Duncan GH (2000) PET studies of the subjective experience of pain. In: Pain imaging (Casey KL, Bushnell MC, eds), pp 123-156. Seattle: IASP.
70. Rausell E, Bae CS, Vinuela A, Huntley GW, Jones EG (1992) Calbindin and parvalbumin cells in monkey VPL thalamic nucleus: distribution, laminar cortical projections, and relations to spinothalamic terminations. J Neurosci 12:4088-4111.
71. Sarlani E, Farooq N, Greenspan JD (2003) Gender and laterality differences in thermosensation throughout the perceptible range. Pain 106:9-18.
72. Schaltenbrand G, Bailey P (1959) Introduction to stereotaxis with an atlas of the human brain. Stuttgart, Germany: Thieme.
73. Sherman SM, Guillery RW (2001) Exploring the thalamus and its role in cortical function. New York: Oxford UP.
74. Soria ED, Fine EJ (1991) Disappearance of thalamic pain after parietal subcortical stroke. Pain 44:285-288.
75. Steriade M, Jones EG, McCormick DA (1997) Thalamus organisation and function. Amsterdam: Elsevier.
76. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. 3D proportional system: an approach to cerebral imaging. Stuttgart, Germany: Georg Thieme Verlag.
77. Tasker RR, Davis KD, Hutchinson WD, Dostrovsky JO (1997) Subcortical and thalamic mapping in functional neurosurgery. In: Stereotactic and functional neurosurgery (Gildenberg PL, Tasker RR, eds), pp 883-923. New York: McGraw-Hill.
78. Torgerson WS, BenDebba M, Mason KJ (1988) Varieties of pain. In: Proceedings of the 5th World Congress on Pain (Dubner R, Gebhart GF, Bond MR, eds), pp 368-374. Amsterdam: Elsevier.
79. Vestergaard K, Nielsen J, Andersen G, Ingeman-Nielsen M, Arendt-Nielsen L, Jensen TS (1995) Sensory abnormalities in consecutive unselected patients with central post-stroke pain. Pain 61:177-186.
80. Vogt BA, Sikes RW (2000) The medial pain system, cingulate cortex, and parallel processing of nociceptive information. Prog Brain Res 122:223-235.
81. White JC, Sweet WH (1969) Pain and the neurosurgeon a forty year experience. Springfield, IL: Charles C Thomas.
82. Willis WD (1985) The pain system. Basel: Karger.
83. Willis Jr WD, Zhang X, Honda CN, Giesler Jr GJ (2001) Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus. Pain 92:267-276.