Physiological changes in primate somatosensory thalamus induced by deafferentation are dependent on the spinal funiculi that are sectioned and time following injury

Neuroscience

Volumn 116, Issue 4, 2003, Pages 1149-1160

  Weng, H R ^a   Lenz, F A ^a   Vierck, C ^b   Dougherty, P M ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Central pain; Monkey; Neuropathic; Spike train

Indexed keywords

ANALYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; DEAFFERENTATION; FEMALE; FORELIMB; MONKEY; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; RECEPTIVE FIELD; SAMPLE; SENSORY NERVE; SOMATOSENSORY CORTEX; SPIKE; SPINAL CORD LESION; SPINAL CORD TRANSSECTION; SPINE; SURVIVAL; SURVIVAL TIME; THALAMUS; VENTRAL ROOT;

EID: 0037470549     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00796-0     Document Type: Article

References (75)

1. Albe-Fessard D., Berkley K.J., Kruger L., Ralston H.J. III, Willis W.D. Jr. Diencephalic mechanisms of pain sensation. Brain Res Rev. 9:1985;217-296.
2. Albe-Fessard D., Lombard M.C. Use of an animal model to evaluate the origin of and protection against deafferentation pain. Adv Pain Res Ther. 5:1983;691-700.
3. Albe-Fessard D., Rampin O. Neurophysiological studies in rats deafferented by dorsal root section. Nashold B.S. Jr, Ovelmen-Levitt J. Deafferentiation pain syndromes pathophysiology and treatment . 1991;125-139 Raven Press, New York.
4. Apkarian A.V., Hodge C.J. A dorsolateral spinothalamic tract in macaque monkey. Pain. 37:1989;323-333.
5. Asmundson G.J.G., Kuperos J.L., Norton G.R. Do patients with chronic pain selectively attend to pain-related information? Preliminary evidence for the mediating role of fear. Pain. 72:1997;27-32.
6. Boivie J., Leijon G. Clinical findings in patients with central poststroke pain. Casey K.L. Pain and central nervous system disease the central pain syndromes . 1991;65-75 Raven Press, New York.
7. Bonica J.J. Introduction semantic, epidemiologic, and educational issues . Casey K.L. Pain and central nervous system disease the central pain syndromes . 1991;13-29 Raven Press, New York.
8. Bushnell M.C., Duncan G.H., Tremblay N. Thalamic VPM nucleus in the behaving monkey. I. Multimodal and discriminative properties of thermosensitive neurons. J Neurophysiol. 69:1993;739-752.
9. Casey K.L., Morrow T.J. Ventral posterior thalamic neurons differentially responsive to noxious stimulation of the awake monkey. Science. 221:1983;675-677.
10. Cesaro P., Mann M.W., Moretti J.L., Defer G., Roualdes B., Nguyen J.P., Degos J.D. Central pain and thalamic hyperactivity a single photon emission computerized tomographic study . Pain. 47:1991;329-336.
11. Chung J.M., Lee K.H., Surmeier D.J., Sorkin L.S., Kim J., Willis W.D. Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. J Neurophysiol. 56:1986;370-390.
12. Craig A.D. A new hypothesis of central pain. Pain Forum. 7:1998;1-14.
13. Davis K.D., Kiss Z.H.T., Tasker R.R., Dostrovsky J.O. Thalamic stimulation-evoked sensations in chronic pain patients and in nonpain (movement disorder) patients. J Neurophysiol. 75:1996;1026-1037.
14. Dechenes M., Paradis M., Roy J.P., Steriade M. Electrophysiology of neurons of lateral thalamic nuclei in cat resting properties and burst discharges . J Neurophysiol. 51:1984;1196-1219.
15. Destexhe A., Contreras D., Steriade M. Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol. 79:1998;999-1016.
16. Dougherty P.M., Lenz F.A. Plasticity of the somatosensory system following neural injury. Boivie J., Hansson P., Lindblom U. Touch, temperature, and pain in health and disease mechanisms and assessments . 1994;439-460 IASP Press, Seattle.
17. Dougherty P.M., Li Y.J., Lenz F.A., Rowland L., Mittman S. Correlation of effects of general anesthetics on somatosensory neurons in the primate thalamus and cortical power. J Neurophysiol. 77:1997;1375-1392.
18. Dougherty P.M., Li Y.J., Lenz F.A., Rowland L., Mittman S. Evidence that excitatory amino acids mediate afferent input to the primate somatosensory thalamus. Brain Res. 278:1997;267-273.
19. Dougherty P.M., Mittman S., Lenz F.A. Facilitation of responses to AMPA but not kainate by cyclothiazide in primate somatosensory thalamus. Neurosci Lett. 245:1998;1-4.
20. Dykes R.W., Sur M., Merzenich M.M., Kaas J.H., Nelson R.J. Regional segregation of neurons responding to quickly adapting, slowly adapting, deep and Pacinian receptors within thalamic ventroposterior lateral and ventroposterior inferior nuclei in the squirrel monkey (Saimiri sciureus). Neuroscience. 6:1981;1687-1692.
21. Faggin B.M., Nguyen K.T., Nicolelis M.A.L. Immediate and simultaneous sensory reorganization at cortical and subcortical levels of the somatosensory system. Proc Natl Acad Sci USA. 94:1997;9428-9433.
22. Guilbaud G., Benoist J.M., Jazat F., Gautron M. Neuronal responsiveness in the ventrobasal thalamic complex of rats with an experimental peripheral mononeuropathy. J Neurophysiol. 64:1990;1537-1554.
23. Han Z.S., Zhang E.T., Craig A.D. Nociceptive and thermoreceptive lamina I neurons are anatomically distinct. Nat Neurosci. 1:1998;218-225.
24. Head H., Holmes G. Sensory disturbances from cerebral lesions. Brain. 34:1912;102-254.
25. Hirato M., Watanabe K., Takahashi A., Hayase N., Horikoshi S., Shibaraki T., Ohye C. Pathophysiology of central (thalamic) pain combined change of sensory thalamus with cerebral cortex around central sulcus . Stereotact Funct Neurosurg. 62:1994;300-303.
26. Iadarola M.J., Max M.B., Berman K.F., Byas-Smith M.G., Coghill R.C., Gracely R.H., Bennett G.J. Unilateral decrease in thalamic activity observed with positron emission tomography in patients with chronic neuropathic pain. Pain. 63:1995;55-64.
27. Ishijima B., Yoshimasu N., Fukushima T., Hori T., Sekino H., Sano K. Nociceptive neurons in the human thalamus. Confin Neurol. 37:1975;99-106.
28. Jahnsen H., Llinas R. Electrophysiological properties of guinea-pig thalamic neurones an in vitro study . J Physiol. 349:1984;205-226.
29. Jeanmonod D., Magnin M., Morel A. Thalamus and neurogenic pain physiological, anatomical, and clinical data . Neuroreport. 4:1993;475-478.
30. Jeanmonod D., Magnin M., Morel A. A thalamic concept of neurogenic pain. Gebhart G.F., Hammond D.L., Jensen T.S. Progress in pain research and management. Proceedings of the 7th world congress on pain, Vol. 2:1994;767-787 IASP Press, Seattle.
31. Kim U., McCormick D.A. Functional and ionic properties of a slow afterhyperpolarization in ferret perigeniculate neurons in vitro. J Neurophysiol. 80:1998;1222-1235.
32. Koyama S., Katayama Y., Maejima S., Hirayama T., Fujii M., Tsubokawa T. Thalamic neuronal hyperactivity following transection of the spinothalamic tract in the cat involvement of N-methyl-D-aspartate receptor . Brain Res. 612:1993;345-350.
33. Krupa D.J., Ghazanfar A.A., Nicolelis M.A.L. Immediate thalamic sensory plasticity depends on corticothalamic feedback. Proc Natl Acad Sci USA. 96:1999;8200-8205.
34. Lenz F.A. The ventral posterior nucleus of thalamus is involved in the generation of central pain syndromes. APS J. 1:1992;42-51.
35. Lenz F.A., Gracely R.H., Baker F.H., Richardson R.T., Dougherty P.M. 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. 399:1998;125-138.
36. Lenz F.A., Hillis A., Gracely R.H., Rowland L.H., Delano M.C., Eckel T.S., Bryan R.N., Dougherty P.M. Subtle neglect of a non-painful part of the body in a chronic pain patient reversed by intralaminar thalamotomy. Soc Neurosci Abstracts. 22:1996;965.
37. Lenz F.A., Kwan H.C., Dostrovsky J.O., Tasker R.R. Characteristics of the bursting pattern of action potentials that occurs in the thalamus of patients with central pain. Brain Res. 496:1989;357-360.
38. Lenz F.A., Kwan H.C., Martin R., Tasker R., Richardson R.T., Dostrovsky J.O. 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. 72:1994;1570-1587.
39. Lenz F.A., Tasker R.P., Dostrovsky J.O., Kwan H.C., Gorecki J., Hirayama T., Murphy J.T. Abnormal single-unit activity recorded in the somatosensory thalamus of a quadriplegic patient with central pain. Pain. 31:1987;225-236.
40. Lenz F.A., Zirh T.A., Garonzick I.M., Richardson R.T., Rowland L.H., Dougherty P.M. Characteristics of spontaneous neuronal activity in the region of human principal sensory nucleus of thalamus in patients with amputations. Neuroscience. 86:1998;1065-1081.
41. Levitt M. Chronic dysesthesias of central neural origin in subhuman primates. Nashold B.S. Jr, Ovelmen-Levitt J. Deafferentation pain syndromes pathophysiology and treatment . 1991;229-238 Raven Press, New York.
42. Lombard M.C., Larabi Y. Electrophysiological study of cervical dorsal horn cells in partially deafferented rats. Adv Pain Res Ther. 5:1983;147-154.
43. Ohara S., Garonzick I., Hua S., Lenz F.A. Studies of the thalamus in patients with central pain and in control patients with movement disorders. Prog Pain Res Clin Manag. 23:2001;219-236.
44. Pearce J., Morley S. An experimental investigation of the construct validity of the McGill Pain Questionnaire. Pain. 39:1989;115-121.
45. Perkel D.H., Gerstein G.I., Moore G.P. Neuronal spike trains and stochastic point processes. I. The single spike train. Biophys J. 7:1967;391-418.
46. Pollin B., Albe-Fessard D. Organization of somatic thalamus in monkeys with and without section of dorsal spinal tracts. Brain Res. 173:1979;431-449.
47. Radhakrishnan V., Tsoukatos J., Davis K.D., Lozano A.M., Dostrovsky J.O. A comparison of the burst activity of lateral thalamic neurons in chronic pain and non-pain patients. Pain. 80:1999;567-575.
48. Ralston D.D., Dougherty P.M., Lenz F.A., Weng H.R., Vierck C.J., Ralston H.J. Plasticity of the inhibitory circuits of the primate ventrobasal thalamus following lesions of the somatosensory pathways. Devor M., Rowbotham M.C., Wiesenfeld-Hallin Z. Proceedings of the 9th world congress on pain. 2000;427-434 IASP Press, Seattle.
49. Ralston H.J. III, Ohara P.T., Meng X.W., Wells J., Ralston D.D. Transneuronal changes of the inhibitory circuitry in the macaque somatosensory thalamus following lesions of the dorsal column nuclei. J Comp Neurol. 371:1996;325-335.
50. Ralston H.J. III, Ralston D.D. Medial lemniscal and spinal projections to the macaque thalamus an electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms . J Neurosci. 14:1994;2485-2502.
51. Rausell E., Bae C.S., Vinuela A., Huntley G.W., Jones E.G. Calbindin and parvalbumin cells in monkey VPL thalamic nucleus distribution, laminar cortical projections, and relations to spinothalamic terminations . J Neurosci. 12:1992;4088-4111.
52. Rodin B.E., Kruger L. Deafferentation in animals as a model for the study of pain an alternative hypothesis . Brain Res Rev. 7:1984;213-228.
53. Sherman S.E., Luo L., Dostrovsky J.O. Altered receptive fields and sensory modalities of rat VPL thalamic neurons during spinal strychnine-induced allodynia. J Neurophysiol. 78:1997;2296-2308.
54. Sherman S.M. Tonic and burst firing dual modes of thalamocortical relay . Trends Neurosci. 24:2001;122-126.
55. Steriade M., Timofev I., Grenier F., Dürmüller N. Role of thalamic and cortical neurons in augmenting responses and self-sustained activity dual intracellular recordings in vivo . J Neurosci. 18:1998;6425-6443.
56. Surmeier D.J., Honda C.N., Willis W.D. Natural groupings of primate spinothalamic neurons based on cutaneous stimulation. Physiological and anatomical features. J Neurophysiol. 59:1988;833-860.
57. Swadlow H.A., Gusev A.G. The impact of "bursting" thalamic impulses at a neocortical synapse. Nat Neurosci. 4:2001;402-408.
58. Szabo J., Cowan W.M. A stereotaxic atlas of the brain of the cynomolgus monkey (Maccaca fascicularis). J Comp Neurol. 222:1984;265-300.
59. Tasker R.R. Deafferentation pain syndromes introduction . Nashold B.S., Ovelmen-Levitt J. Deafferentation pain syndromes pathophysiology and treatment . 1991;241-257 Raven Press, New York.
60. Timofev I., Steriade M. Cellular mechanisms underlying intrathalamic augmenting responses of reticular and relay neurons. J Neurophysiol. 79:1998;2716-2729.
61. Tremblay N., Bushnell M.C., Duncan G.H. Thalamic VPM nucleus in the behaving monkey. II. Response to air-puff stimulation during discrimination and attention tasks. J Neurophysiol. 69:2002;753-763.
62. Tsoukatos J.D., Davis K.D., Tasker R.R., Lozano A.M., Dostrovsky J.O. Deafferentation and local damage give rise to bursting activity in thalamus of awake patients. Neurosci Abstr. 22:1996;98.
63. Vierck CJ, Greenspan JD, Ritz LA (1990) Long-term changes in purposive and reflexive responses to nociceptive stimulation following anterolateral chordotomy. J Neurosci 10:2077-2095.
64. Vierck C.J., Hamilton D.M., Thornby J.I. Pain reactivity of monkeys after lesions to the dorsal and lateral columns of the spinal cord. Exp Brain Res. 13:1971;140-158.
65. Vierck C.J. Jr. Impaired detection of repetitive stimulation following interruption of the dorsal spinal column in monkeys. Somatosens Motor Res. 15:1998;157-163.
66. Vierck C.J. Jr, Cohen R.H., Cooper B.Y. Effects of spinal tractotomy on spatial sequence recognition in macaques. J Neurosci. 3:1983;280-290.
67. Vierck C.J. Jr, Greenspan J.D., Ritz L.A. Long-term changes in purposive and reflexive responses to nociceptive stimulation following anterolateral chordotomy. J Neurosci. 10:1990;2077-2095.
68. Vierck C.J. Jr, 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. 102:1979;233-248.
69. Wall P.D. Alterations in the central nervous system after deafferentation connectivity control . Bonica J.J. Advances in pain research and therapy. 1983;677-689 Raven Press, New York.
70. Wall P.D., Egger M.D. Formation of new connexions in adult rat brains after partial deafferentation. Nature. 232:1971;542-545.
71. Warren R.A., Agmon A., Jones E.G. Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro. J Neurophysiol. 72:1994;1993-2003.
72. Watanabe Y., Saito H., Abe K. Tricyclic antidepressants block NMDA receptor-mediated synaptic responses and induction of long-term potentiation in rat hippocampal slices. Neuropharmacology. 32:1993;479-486.
73. Weng H.R., Lee J.I., Lenz F.A., Schwartz A., Vierck C., Rowland L., Dougherty P.M. Functional plasticity in primate somatosensory thalamus following chronic lesion of the ventral lateral spinal cord. Neuroscience. 101:2000;393-401.
74. Willis W.D. The pain system the neural basis of nociceptive transmission in the mammalian nervous system . 1985;Karger, Basel.
75. Zhang X., Wenk H.N., Honda C.N., Giesler G.J. Jr. Locations of spinothalamic tract axons in cervical and thoracic spinal cord white matter in monkeys. J Neurophysiol. 83:2000;2869-2880.