- Email: [email protected]
Will Ventralis Intermedius Deep Brain Stimulation for Tremor Be Replaced by Posterior Subthalamic Area or Caudal Zona Incerta Stimulation?
Perspectives Commentary on: Reoperation After Failed Deep Brain Stimulation for Essential Tremor by Blomstedt et al. pp. 554.E1-554.E5.
Takaomi Taira, M.D., Ph.D. Director of Stereotactic and Functional Neurosurgery Department of Neurosurgery Tokyo Women’s Medical University
Will Ventralis Intermedius Deep Brain Stimulation for Tremor Be Replaced by Posterior Subthalamic Area or Caudal Zona Incerta Stimulation? Takaomi Taira
N
eurosurgical management of tremor has a very long history. Pioneer neurosurgeons were making lesions, with open surgery without an operative microscope, at different levels in the pyramidal tract to stop tremor by sacrificing normal motor function. Bucy (3) performed the first excision of the primary motor cortex in 1937 to control tremor. Walker (24) performed midbrain pedunculotomy in 1949, and Putnam (20) cut the spinal pyramidal tract. Today, even young residents consider that such approaches to the pyramidal tract to relieve involuntary movements are nonsense. However, I believe these neurosurgical giants were very serious, and no one was able to question the value of such pyramidal tract surgery for tremor. Meyers was the first surgeon to approach the pallidofugal fibers to control parkinsonian symptoms; this was done under macroscopic open craniotomy, and the mortality rate was high (4). The story of discovery of “ligation of the anterior choroidal artery” for parkinsonism is well known and interesting. When Cooper was approaching to the midbrain peduncle for pedunculotomy, he accidentally injured the anterior choroidal artery and clipped it. He gave up the operation and closed the wound. The parkinsonian patient, after recovery from anesthesia, showed no Parkinson symptoms, and there was no motor paresis. Based on this experience, Cooper started performing “anterior choroidal artery ligation” for parkinsonism. Cooper relates the story of this discovery in detail in his book, The Vital Probe (5); this is “a must read” to know an untold history of neurosurgical management of movement disorders. Stereotactic surgery was first performed by Spiegel and Wycis 1947, not for movement disorders but to control psychiatric disorders. When Narabayashi et al. (18) reported “procaine oil pallidotomy” for parkinsonian rigidity and tremor in 1956, Spiegel and Wycis (21) criticized Narabayashi, stating that “not even mentioning a single word the fact we have reported such operations since
Key words 䡲 DBS 䡲 Posterior subthalamic area 䡲 Tremor 䡲 Vim 䡲 Zona incerta
Abbreviations and Acronyms cZI: Caudal zona incerta DBS: Deep brain stimulation PSA: Posterior subthalamic area STN: Subthalamic nucleus Vim: Ventralis intermedius
WORLD NEUROSURGERY 78 [5]: 445-446, NOVEMBER 2012
1949,” and “they also describe a stereoencephalotome that is merely an imitation of our apparatus.” Narabayashi responded, “We believe selective pallidal invasion in Parkinsonism is our innovation.” He also explained the device was not an imitation, which was later unanimously accepted (16). The stereotactic target for tremor control moved from the pallidum to the thalamus in the 1960s and 1970s mainly based on the work by Hassler et al. (8-10), and Cooper et al. (6, 7). In those days, the motor thalamus had just been named the ventrolateral thalamus, and there was no clear subclassification especially in cases of stereotactic surgery. The localization and lesioning procedures were not sophisticated enough to make a tiny selective lesion in the ventrolateral thalamus. Ohye’s team established that small selective lesioning in the posterior part of the ventrolateral thalamus (ventralis intermedius [Vim]) was enough to control tremor (11, 17, 19). Since then, the Vim nucleus of the thalamus has been regarded as a gold standard target not only for parkinsonian tremor but also for other various types of tremor including essential tremor. However, a survey by Laitinen in 1985 (15) about stereotactic targets for Parkinson disease showed considerable variability among prominent stereotactic specialists. Even before the era of modern pallidotomy and deep brain stimulation (DBS), some neurosurgeons targeted the zona incerta, subthalamic area, and Forel field. Because magnetic resonance imaging and computed tomography scan were not readily available, validation of the actual location of the lesion was impossible in those days. Introduction of DBS for tremor control in the 1990s gained popularity mainly because of its reversibility and lesser chance of complications. Initially, DBS was considered the same as lesioning in terms of stereotactic targeting, and the traditional Vim target was chosen for tremor control by DBS. However,
Department of Neurosurgery, Tokyo Women’s Medical University, Tokyo, Japan To whom correspondence should be addressed: Takaomi Taira, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2012) 78, 5:445-446. DOI: 10.1016/j.wneu.2012.01.025
www.WORLDNEUROSURGERY.org
445
PERSPECTIVES
there are some reports on mismatch between DBS and thalamotomy, which suggests different mechanisms of effect of DBS and thalamotomy (12). DBS of the subthalamic nucleus (STN) for Parkinson disease also has a strong antitremor effect. However, it is still controversial whether stimulation to the STN itself or stimulation to the zona incerta adjacent to the STN is responsible for tremor suppression. In the early 1970s, Velasco et al. (22, 23) had already noticed that a small lesion in the subthalamic area is very effective to control tremor. After introduction of DBS, his team started stimulation of this area with what they called “subthalamic prelemniscal radiation.” Kitagawa et al. (13, 14) found that stimulation of this area, known as the posterior subthalamic area (PSA), is effective for proximal tremor that is generally resistant to Vim stimulation. Blomstedt et al. (1, 2) have been actively studying PSA DBS, showing that PSA is a more effective target to control tremor than Vim. In this issue of WORLD NEUROSURGERY, Blomstedt et al. report on reoperation after failed DBS for essential tremor. In their report, before the reoperation, Vim DBS showed an improvement of 25% in hand function and tremor in the treated hand, whereas caudal zona incerta (cZi) DBS achieved an improvement of 57%. The authors also noted the effect was modest in patients with deterioration many years after the initial operation, suggesting superiority of cZi stimulation.
REFERENCES
There are several nomenclatures in these reports: subthalamic prelemniscal radiation, posterior subthalamic area, and cZi. This varied nomenclature may be confusing. The cZi target is a more focused area in the PSA, and, as reported by Blomstedt et al., it is slightly posterior-medial to the tail of the STN at the level of the maximal diameter of the red nucleus. However, there are still many questions to be answered. Is cZi superior to other areas in the PSA? Are there any differences in targets and clinical effects in reported PSA, cZi, or prelemniscal DBS? Are the reports saying the same thing? Is there any variation of cZi target based on anterior commissure-posterior commissure coordinates? The definition of nomenclature is also important. From where to where is the PSA or cZi? I think that one disadvantage of exploring this target is that the area is silent with microelectrode recordings because it is basically a white matter area. It is also important to ask the question is the Vim target really in the Vim? Ohye, after extensive study of the Vim nucleus of the thalamus, said that there is a “real sweet spot” for tremor control in the most lateral part of the so-called Vim that might be outside the somatotopic arrangement of the Vim. Ohye used 16 –18 mm for laterality of the Vim target in his final years. I consider that the PSA or the cZi is a very promising target for intractable tremor, and it may become the first choice in the near future.
anatomical and clinical data. Confin Neurol 32:79-87, 1970.
1. Blomstedt P, Sandvik U, Hariz MI, Fytagoridis A, Forsgren L, Hariz GM, Koskinen LO: Influence of age, gender and severity of tremor on outcome after thalamic and subthalamic DBS for essential tremor. Parkinsonism Relat Disord 17:617-620, 2011.
10. Hassler R, Riechert T, Mundinger F, Umbach W, Ganglberger JA: Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 83:337-350, 1960.
2. Blomstedt P, Sandvik U, Tisch S: Deep brain stimulation in the posterior subthalamic area in the treatment of essential tremor. Mov Disord 25:1350-1356, 2010.
11. Hirai T, Miyazaki M, Nakajima H, Shibazaki T, Ohye C: The correlation between tremor characteristics and the predicted volume of effective lesions in stereotaxic nucleus ventralis intermedius thalamotomy. Brain 106(Pt 4):1001-1018, 1983.
3. Bucy PC: Surgical relief of tremor at rest. Ann Surg 122:933-941, 1945. 4. Cooper I: The Neurosurgical Alleviation of Parkinsonism. Springfield, IL: Charles C Thomas; 1956. 5. Cooper IS: The Vital Probe: My Life as a Brain Surgeon. New York: WW Norton & Co; 1981. 6. Cooper IS, Bravo GJ: Implications of a five-year study of 700 basal ganglia operations. Neurology 8:701-707, 1958 7. Cooper IS, Bravo GJ, Riklan M, Davidson NW, Gorek EA: Chemopallidectomy and chemothalamectomy for parkinsonism. Geriatrics 13:127-147, 1958. 8. Hassler R, Mundinger F, Riechert T: Correlations between clinical and autoptic findings in stereotaxic operations of parkinsonism. Confin Neurol 26:282290, 1965. 9. Hassler R, Mundinger F, Riechert T: Pathophysiology of tremor at rest derived from the correlation of
446
www.SCIENCEDIRECT.com
12. Kiss ZH, Wilkinson M, Krcek J, Suchowersky O, Hu B, Murphy WF, Hobson D, Tasker RR: Is the target for thalamic deep brain stimulation the same as for thalamotomy? Mov Disord 18:1169-1175, 2003. 13. Kitagawa M, Fukushima J, Tashiro K: Relationship between antisaccades and the clinical symptoms in Parkinson’s disease. Neurology 44:2285-2289, 1994. 14. Kitagawa M, Murata J, Uesugi H, Kikuchi S, Saito H, Tashiro K, Sawamura Y: Two-year follow-up of chronic stimulation of the posterior subthalamic white matter for tremor-dominant Parkinson’s disease. Neurosurgery 56:281-289, 2005. 15. Laitinen LV: Brain targets in surgery for Parkinson’s disease: results of a survey of neurosurgeons. J Neurosurg 62:349-351, 1985.
17. Narabayashi H, Ohye C: Nucleus ventralis intermedius of human thalamus. Transactions of the American Neurological Association 99:232-233, 1974. 18. Narabayashi H, Okuma T, Shikiba S: Procaine oil blocking of the globus pallidus. AMA Arch Neurol Psychiatry 75:36-48, 1956. 19. Ohye C, Maeda T, Narabayashi H: Physiologically defined VIM nucleus: its special reference to control of tremor. Appl Neurophysiol 39:285-295, 1976. 20. Putnam TJ: The surgical treatment of the dyskinesias. Folia Psychiatr Neurol Neurochir Neerlandica 53:387-391, 1950. 21. Spiegel EA, Wycis HT: Correspondense: procaine oil blocking of globus pallidus. AMA Arch Neurol Psychiatry 76:263, 1956. 22. Velasco F, Velasco M, Machado JP: A statisticl outline of the subthalamic target for the arrest of tremor. Appl Neurophysiol 38:38-46, 1975. 23. Velasco FC, Molina-Negro P, Bertrand C, Hardy J: Further definition of the subthalamic target for arrest of tremor. J Neurosurg 36:184-191, 1972. 24. Walker AE: Cerebral pedunculotomy for the relief of involuntary movements; hemiballismus. Acta Psychiatr Neurol 24:723-729, 1949. Citation: World Neurosurg. (2012) 78, 5:445-446. DOI: 10.1016/j.wneu.2012.01.025 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
16. Narabayashi H: Beginning and development of stereotaxic surgery in Tokyo. Confin Neurol 37:364373, 1975.
1878-8750/$ - see front matter © 2012 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2012.01.025
Takaomi Taira, M.D., Ph.D. Director of Stereotactic and Functional Neurosurgery Department of Neurosurgery Tokyo Women’s Medical University
Will Ventralis Intermedius Deep Brain Stimulation for Tremor Be Replaced by Posterior Subthalamic Area or Caudal Zona Incerta Stimulation? Takaomi Taira
N
eurosurgical management of tremor has a very long history. Pioneer neurosurgeons were making lesions, with open surgery without an operative microscope, at different levels in the pyramidal tract to stop tremor by sacrificing normal motor function. Bucy (3) performed the first excision of the primary motor cortex in 1937 to control tremor. Walker (24) performed midbrain pedunculotomy in 1949, and Putnam (20) cut the spinal pyramidal tract. Today, even young residents consider that such approaches to the pyramidal tract to relieve involuntary movements are nonsense. However, I believe these neurosurgical giants were very serious, and no one was able to question the value of such pyramidal tract surgery for tremor. Meyers was the first surgeon to approach the pallidofugal fibers to control parkinsonian symptoms; this was done under macroscopic open craniotomy, and the mortality rate was high (4). The story of discovery of “ligation of the anterior choroidal artery” for parkinsonism is well known and interesting. When Cooper was approaching to the midbrain peduncle for pedunculotomy, he accidentally injured the anterior choroidal artery and clipped it. He gave up the operation and closed the wound. The parkinsonian patient, after recovery from anesthesia, showed no Parkinson symptoms, and there was no motor paresis. Based on this experience, Cooper started performing “anterior choroidal artery ligation” for parkinsonism. Cooper relates the story of this discovery in detail in his book, The Vital Probe (5); this is “a must read” to know an untold history of neurosurgical management of movement disorders. Stereotactic surgery was first performed by Spiegel and Wycis 1947, not for movement disorders but to control psychiatric disorders. When Narabayashi et al. (18) reported “procaine oil pallidotomy” for parkinsonian rigidity and tremor in 1956, Spiegel and Wycis (21) criticized Narabayashi, stating that “not even mentioning a single word the fact we have reported such operations since
Key words 䡲 DBS 䡲 Posterior subthalamic area 䡲 Tremor 䡲 Vim 䡲 Zona incerta
Abbreviations and Acronyms cZI: Caudal zona incerta DBS: Deep brain stimulation PSA: Posterior subthalamic area STN: Subthalamic nucleus Vim: Ventralis intermedius
WORLD NEUROSURGERY 78 [5]: 445-446, NOVEMBER 2012
1949,” and “they also describe a stereoencephalotome that is merely an imitation of our apparatus.” Narabayashi responded, “We believe selective pallidal invasion in Parkinsonism is our innovation.” He also explained the device was not an imitation, which was later unanimously accepted (16). The stereotactic target for tremor control moved from the pallidum to the thalamus in the 1960s and 1970s mainly based on the work by Hassler et al. (8-10), and Cooper et al. (6, 7). In those days, the motor thalamus had just been named the ventrolateral thalamus, and there was no clear subclassification especially in cases of stereotactic surgery. The localization and lesioning procedures were not sophisticated enough to make a tiny selective lesion in the ventrolateral thalamus. Ohye’s team established that small selective lesioning in the posterior part of the ventrolateral thalamus (ventralis intermedius [Vim]) was enough to control tremor (11, 17, 19). Since then, the Vim nucleus of the thalamus has been regarded as a gold standard target not only for parkinsonian tremor but also for other various types of tremor including essential tremor. However, a survey by Laitinen in 1985 (15) about stereotactic targets for Parkinson disease showed considerable variability among prominent stereotactic specialists. Even before the era of modern pallidotomy and deep brain stimulation (DBS), some neurosurgeons targeted the zona incerta, subthalamic area, and Forel field. Because magnetic resonance imaging and computed tomography scan were not readily available, validation of the actual location of the lesion was impossible in those days. Introduction of DBS for tremor control in the 1990s gained popularity mainly because of its reversibility and lesser chance of complications. Initially, DBS was considered the same as lesioning in terms of stereotactic targeting, and the traditional Vim target was chosen for tremor control by DBS. However,
Department of Neurosurgery, Tokyo Women’s Medical University, Tokyo, Japan To whom correspondence should be addressed: Takaomi Taira, M.D., Ph.D. [E-mail: [email protected]] Citation: World Neurosurg. (2012) 78, 5:445-446. DOI: 10.1016/j.wneu.2012.01.025
www.WORLDNEUROSURGERY.org
445
PERSPECTIVES
there are some reports on mismatch between DBS and thalamotomy, which suggests different mechanisms of effect of DBS and thalamotomy (12). DBS of the subthalamic nucleus (STN) for Parkinson disease also has a strong antitremor effect. However, it is still controversial whether stimulation to the STN itself or stimulation to the zona incerta adjacent to the STN is responsible for tremor suppression. In the early 1970s, Velasco et al. (22, 23) had already noticed that a small lesion in the subthalamic area is very effective to control tremor. After introduction of DBS, his team started stimulation of this area with what they called “subthalamic prelemniscal radiation.” Kitagawa et al. (13, 14) found that stimulation of this area, known as the posterior subthalamic area (PSA), is effective for proximal tremor that is generally resistant to Vim stimulation. Blomstedt et al. (1, 2) have been actively studying PSA DBS, showing that PSA is a more effective target to control tremor than Vim. In this issue of WORLD NEUROSURGERY, Blomstedt et al. report on reoperation after failed DBS for essential tremor. In their report, before the reoperation, Vim DBS showed an improvement of 25% in hand function and tremor in the treated hand, whereas caudal zona incerta (cZi) DBS achieved an improvement of 57%. The authors also noted the effect was modest in patients with deterioration many years after the initial operation, suggesting superiority of cZi stimulation.
REFERENCES
There are several nomenclatures in these reports: subthalamic prelemniscal radiation, posterior subthalamic area, and cZi. This varied nomenclature may be confusing. The cZi target is a more focused area in the PSA, and, as reported by Blomstedt et al., it is slightly posterior-medial to the tail of the STN at the level of the maximal diameter of the red nucleus. However, there are still many questions to be answered. Is cZi superior to other areas in the PSA? Are there any differences in targets and clinical effects in reported PSA, cZi, or prelemniscal DBS? Are the reports saying the same thing? Is there any variation of cZi target based on anterior commissure-posterior commissure coordinates? The definition of nomenclature is also important. From where to where is the PSA or cZi? I think that one disadvantage of exploring this target is that the area is silent with microelectrode recordings because it is basically a white matter area. It is also important to ask the question is the Vim target really in the Vim? Ohye, after extensive study of the Vim nucleus of the thalamus, said that there is a “real sweet spot” for tremor control in the most lateral part of the so-called Vim that might be outside the somatotopic arrangement of the Vim. Ohye used 16 –18 mm for laterality of the Vim target in his final years. I consider that the PSA or the cZi is a very promising target for intractable tremor, and it may become the first choice in the near future.
anatomical and clinical data. Confin Neurol 32:79-87, 1970.
1. Blomstedt P, Sandvik U, Hariz MI, Fytagoridis A, Forsgren L, Hariz GM, Koskinen LO: Influence of age, gender and severity of tremor on outcome after thalamic and subthalamic DBS for essential tremor. Parkinsonism Relat Disord 17:617-620, 2011.
10. Hassler R, Riechert T, Mundinger F, Umbach W, Ganglberger JA: Physiological observations in stereotaxic operations in extrapyramidal motor disturbances. Brain 83:337-350, 1960.
2. Blomstedt P, Sandvik U, Tisch S: Deep brain stimulation in the posterior subthalamic area in the treatment of essential tremor. Mov Disord 25:1350-1356, 2010.
11. Hirai T, Miyazaki M, Nakajima H, Shibazaki T, Ohye C: The correlation between tremor characteristics and the predicted volume of effective lesions in stereotaxic nucleus ventralis intermedius thalamotomy. Brain 106(Pt 4):1001-1018, 1983.
3. Bucy PC: Surgical relief of tremor at rest. Ann Surg 122:933-941, 1945. 4. Cooper I: The Neurosurgical Alleviation of Parkinsonism. Springfield, IL: Charles C Thomas; 1956. 5. Cooper IS: The Vital Probe: My Life as a Brain Surgeon. New York: WW Norton & Co; 1981. 6. Cooper IS, Bravo GJ: Implications of a five-year study of 700 basal ganglia operations. Neurology 8:701-707, 1958 7. Cooper IS, Bravo GJ, Riklan M, Davidson NW, Gorek EA: Chemopallidectomy and chemothalamectomy for parkinsonism. Geriatrics 13:127-147, 1958. 8. Hassler R, Mundinger F, Riechert T: Correlations between clinical and autoptic findings in stereotaxic operations of parkinsonism. Confin Neurol 26:282290, 1965. 9. Hassler R, Mundinger F, Riechert T: Pathophysiology of tremor at rest derived from the correlation of
446
www.SCIENCEDIRECT.com
12. Kiss ZH, Wilkinson M, Krcek J, Suchowersky O, Hu B, Murphy WF, Hobson D, Tasker RR: Is the target for thalamic deep brain stimulation the same as for thalamotomy? Mov Disord 18:1169-1175, 2003. 13. Kitagawa M, Fukushima J, Tashiro K: Relationship between antisaccades and the clinical symptoms in Parkinson’s disease. Neurology 44:2285-2289, 1994. 14. Kitagawa M, Murata J, Uesugi H, Kikuchi S, Saito H, Tashiro K, Sawamura Y: Two-year follow-up of chronic stimulation of the posterior subthalamic white matter for tremor-dominant Parkinson’s disease. Neurosurgery 56:281-289, 2005. 15. Laitinen LV: Brain targets in surgery for Parkinson’s disease: results of a survey of neurosurgeons. J Neurosurg 62:349-351, 1985.
17. Narabayashi H, Ohye C: Nucleus ventralis intermedius of human thalamus. Transactions of the American Neurological Association 99:232-233, 1974. 18. Narabayashi H, Okuma T, Shikiba S: Procaine oil blocking of the globus pallidus. AMA Arch Neurol Psychiatry 75:36-48, 1956. 19. Ohye C, Maeda T, Narabayashi H: Physiologically defined VIM nucleus: its special reference to control of tremor. Appl Neurophysiol 39:285-295, 1976. 20. Putnam TJ: The surgical treatment of the dyskinesias. Folia Psychiatr Neurol Neurochir Neerlandica 53:387-391, 1950. 21. Spiegel EA, Wycis HT: Correspondense: procaine oil blocking of globus pallidus. AMA Arch Neurol Psychiatry 76:263, 1956. 22. Velasco F, Velasco M, Machado JP: A statisticl outline of the subthalamic target for the arrest of tremor. Appl Neurophysiol 38:38-46, 1975. 23. Velasco FC, Molina-Negro P, Bertrand C, Hardy J: Further definition of the subthalamic target for arrest of tremor. J Neurosurg 36:184-191, 1972. 24. Walker AE: Cerebral pedunculotomy for the relief of involuntary movements; hemiballismus. Acta Psychiatr Neurol 24:723-729, 1949. Citation: World Neurosurg. (2012) 78, 5:445-446. DOI: 10.1016/j.wneu.2012.01.025 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
16. Narabayashi H: Beginning and development of stereotaxic surgery in Tokyo. Confin Neurol 37:364373, 1975.
1878-8750/$ - see front matter © 2012 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2012.01.025