Pathways involved in thalamic ventrobasal stimulation for pain relief: evidence against the hypothesis VB stimulation -> rostroventral medulla excitation -> dorsal horn inhibition

Vias envolvidas no alívio da dor pela estimulação talâmica ventrobasal: evidência contra a hipótese estimulação ventrobasal --> excitação do bulbo rostroventral -> inibição do corno dorsal

Pathways involved in thalamic ventrobasal stimulation for pain relief: evidence against the hypothesis VB stimulation ® rostroventral medulla excitation ® dorsal horn inhibition

Vias envolvidas no alívio da dor pela estimulação talâmica ventrobasal: evidência contra a hipótese estimulação ventrobasal ® excitação do bulbo rostroventral ® inibição do corno dorsal

Osvaldo Vilela Filho^I; Ronald. R. Tasker^II

^IM.D. Head, Division of Neurosurgery, Instituto Ortopédico de Goiânia. Ex-Clinical Research Fellow, Division of Neurosurgery, The Toronto Hospital, Western Division; Department of Surgery, University of Toronto

^IIM.D., Division of Neurosurgery, The Toronto Hospital, Western Division; Department of Surgery, University of Toronto. Paper prepared at the Division of Neurosurgery, The Toronto Hospital, Western Division; Departament of Surgery, University of Toronto

SUMMARY

Despite its use for a long time, the way thalamic ventrobasal (VB) stimulation acts to produce pain relief is still unknown. One of the most accepted hypotheses, sponsored by Tsubokawa among others, proposes that VB stimulation excites raphespinal and reticulospinal neurons of the rostroventral medulla which in turn send respectively inhibitory serotonergic and noradrenergic axons through both dorsolateral funiculi (DLF) to the dorsal horn ( DH) nociceptive neurons; this pathway would be the same as is involved in periventricular-periaqueductal gray (PVG-PAG) stimulation induced inhibition of DH nociceptive neurons. This hypothesis implicates the necessity of DLF intactness; in fact, it was showed that section of bilateral DLF inhibits the response of DH nociceptive neurons to VB stimulation. If the above mentioned hypothesis is correct, one could expect that unilateral VB stimulation would produce bilateral pain relief, VB and PVG stimulation would be useful for treating the same modalities of pain and that in patients with central cord-based pain harboring complete cord transection, VB stimulation would not work at all. In order to check these possibilities, the patiens with central cord-based pain admitted to the Division of Neurosurgery, Toronto Hospital between June 1978 and July 1991 to undergo deep brain stimulation (DBS) were reviewed. Sixteen patients were operated on. Based on clinical criteria, four out of these sixteen patients were thought to present complet cord transection (all four were men, with an average age of 48 years and pain secondary to cord injury). The effectiveness of the procedure was evaluated in this subset of patients: 75% of them enjoyed excellent pain relief with VB stimulation; PVG stimulation, however, performed in three out of these four patients, did not produce pain relief. Besides, our clinical experience has demonstrated that VB stimulation is effective in treating only contralateral pain.These results, as well as certain experimental data provided by a review of the literature, seem to provide evidence enough to contest Tsubokawa's hypothesis.

Key words: pain, analgesia, electrical stimulation therapy, thalamic nuclei, thalamus, stereotaxis.

RESUMO

A despeito de seu uso há longo tempo, a maneira pela qual a estimulação talâmica ventrobasal (VB) produz alívio da dor é ainda desconhecida. Segundo uma das hipóteses mais aceitas, defendida por Tsubokawa dentre outros, a estimulação de VB excita neurônios rafe-espinhais e reticulo-espinhais do bulbo rostroventral, os quais por sua vez emitem respectivamente axônios serotoninérgicos e noradrenérgicos inibitórios para os neurônios nociceptivos de ambos os cornos dorsais através dos funículos dorsolaterais da medula espinhal; essa via é a mesma proposta para a inibição dos neurônios nociceptivos dos cornos dorsais pela estimulação da substância cinzenta periventricular-periaquedutal (PVG-PAG). Tal hipótese, obviamente, subentende a necessidade da integridade dos funículos dorsolaterais da medula; de fato, já foi demonstrado que a secção desses funículos inibe a resposta dos neurônios nociceptivos dos cornos dorsais à estimulação de VB. Se a hipótese mencionada for correta, poder-se-á esperar que: (1) a estimulação unilateral de VB produza alívio bilateral da dor; (2) a estimulação de VB e PVG-PAG sejam úteis para tratar as mesmas modalidades de dor; (3) a estimulação de VB seja ineficaz em pacientes com secção medular completa apresentando dor central de origem medular. Para se avaliar essas possibilidades, foram revistos os pacientes com dor central de origem medular admitidos à Divisão de Neurocirurgia do Toronto Hospital entre junho 1978 e julho 1991 para serem submetidos à estimulação cerebral profunda. Dezesseis pacientes foram operados nesse período, quatro dos quais apresentavam lesão medular completa, segundo critérios clínicos. Todos eram homens, com média de idade de 48 anos e com dor secundária a traumatismo raquimedular. A eficácia da estimulação cerebral profunda foi avaliada nesse subgrupo de pacientes: 75% deles (3 dentre 4) apresentaram excelente alívio da dor à estimulação de VB; a estimulação de PVG, porém, realizada em três desses quatro pacientes, foi ineficaz em todos eles. Além disso, a experiência clínica tem demonstrado que a estimulação unilateral de VB só é eficaz para o tratamento de dor contralateral. Esses resultados, bem como certos achados experimentais fornecidos pela revisão da literatura, parecem prover evidência suficiente para contestar a hipótese de Tsubokawa.

Palavras-chave: dor, analgesia, estimulação elétrica, núcleos talâmicos, tálamo, estereotaxia.

Texto completo disponível apenas em PDF.

Full text available only in PDF format.

Acknowledgments - The authors thank the architect Dimas Aidar, for the illustration, and the colleagues Dr. Andrew Parrent, Dr. Joaquim Tomé de Sousa, Dr. Herbert A. Oliveira e Souza and Dr. Umberto Ferreira, for their critical review of this paper.

Aceite: 5-janeiro-1994.

Dr. Osvaldo Vilela Filho - Rua T 38,912/ Apt 302, Setor Bueno - 74230-070 - Goiânia GO - Brasil.

• 1. Adams JE, Hosobuchi Y, Fields HL. Stimulation of internal capsule for relief of chronic pain. J Neurosurg 1974, 41: 740-744.
• 2. Aiko Y, Shima F, Hosokawa S, Kato M, Kitamura K. Altered local cerebral glucose utilization induced by electrical stimulations of the thalamic sensory and parafascicular nuclei in rats. Brain Res 1987, 408: 47-56.
• 3. Bárbaro NM, Fields HL. Physiological anatomy of pain. In Youmans JR (ed). Neurological surgery. Philadelphia: Saunders 1990, Vol 6, p 3785-3802.
• 4. Benabid AL, Henriksen SJ, McGinty JF, Bloom FE. Thalamic nucleus ventro-postero-lateralis inhibits nucleus parafascicularis response to noxious stimuli through a non-opioid pathway. Brain Res 1983, 280:217-231.
• 5. Bonica JJ, Yaksh T, Liebeskind JC, Pechnick RN, DePaulis A. Biochemistry and modulation of nociception and pain. In Bonica JJ (ed). The management of pain. Philadelphia: Lea and Febiger 1990, Vol 1, p 95-121.
• 6. Duncan GH, Bushnell MC, Marchand S. Deep brain stimulation: a review of basic research and clinical studies. Pain 1991, 45: 49-59.
• 7. Gerhart KD, Yezierski RP, Fang ZR, Willis WD: Inhibition of primate spinothalamic tract neurons by stimulation in ventral posterior lateral (VPL) thalamic nucleus: possible mechanisms. J Neurophysiol 1983, 49: 406-423.
• 8. Hosobuchi Y. Intracerebral stimulation for the relief of chronic pain. In Youmans JR (ed). Neurological surgery. Philadelphia: Saunders 1990, Vol 6, p 4128-4143.
• 9. Hosobuchi Y. Subcortical electrical stimulation for control of intractable pain in humans. J Neurosurg 1986,  64: 543-553.
• 10. Levy RM, Lamb S, Adams JE. Treatment of chronic pain by deep brain stimulation: long term follow-up and review of the literature. Neurosurgery 1987, 21: 885-893.
• 11. Levy RM, Lamb S, Adams JE. Deep brain stimulation for chronic pain: long-term results and complications. In Lunsford LD (ed). Modern stereotactic neurosurgery. Boston: Martinus Nijhoff 1988, p 395-407.
• 12. Mazars G, Merienne L, Cioloca C. Traitement de certains types de douleurs par des stimulations talamiques implantables. Neurochimia 1974, 20: 117-124.
• 13. Tasker RR. Pain resulting from central nervous system pathology (central pain). In Bonica JJ (ed). The management of pain. Philadelphia: Lea and Febiger, 1990, Vol 1, p 264-283.
• 14. Tasker RR, Lenz F, Yamashiro K, Gorecki J, Hirayama T, Dostrovsky JO. Microelectrode technics in localization of stereotactic targets. Neurol Res 1987, 9: 105-112.
• 15. Tsubokawa T, Yamamoto T, Katayama Y, Moriyasu N. Clinical results and physiological basis of thalamic relay nucleus stimulation for relief of intractable pain with morphine tolerance. Appl Neurophysiol 1982,45: 143-155.
• 16. Tsubokawa T, Yamamoto T, Katayama Y, Hirayama T, Sibuya H. Thalamic relay nucleus stimulation for relief of intractable pain: clinical results and B-endorphin immunoreactivity in the cerebrospinal fluid. Pain 1984, 18: 115-126.
• 17. Tsubokawa T, Katayama Y, Yamamoto T, Hirayama T. Deafferentation pain and stimulation of the thalamic sensory relay nucleus: clinical and experimental study. Appl Neurophysiol 1985, 48: 166-171.
• 18. Tsubokawa T. Chronic stimulation of deep brain structures for treatment of chronic pain: clinical significance and surgical indications. In Tasker RR (ed). Neurosurgery: stereotactic surgery. Philadelphia: Hanley & Belfus 1987,  Vol 2, No l,p 235-255.
• 19. Willis WD, Gerhart KD, Willcockson WS, Yezierski RP, Wilcox TK, Cargill CL. Primate raphe and reticulospinal neurons: effects of stimulation in periaqueductal gray or VPLc thalamic nucleus. J Neurophysiol 1984, 51: 467- 480.

Publication Dates

• Publication in this collection
  19 Jan 2011
• Date of issue
  Sept 1994