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Electrophysiological interpretations of the clinical response to stimulation parameters of pallidal deep brain stimulation for cervical dystonia

  • Clinical Article - Functional
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Abstract

Objective

Deep brain stimulation (DBS) at the posterolateral ventral portion of the globus pallidus internus (GPi) has been regarded as a good therapeutic modality. Because the theoretical principle behind the stimulation parameters is yet to be determined, this study aimed to interpret analyses of the stimulation parameters used in our department based on an electrophysiological review.

Methods

Nineteen patients with medically refractory idiopathic cervical dystonia who underwent GPi DBS were enrolled. The baseline and follow-up parameters were analyzed according to their dependence on time after DBS. The pattern of changes in the stimulation parameters over time, the differences across the four active contacts, and the relationship between the stimulation parameters and clinical benefits were evaluated.

Results

Mean age and disease duration were 50.9 years and 54.7 months, respectively. Mean follow-up duration was 22.6 months. The amplitude and frequency exhibited significant increasing temporal patterns, i.e., a mean amplitude and frequency of 3.1 V and 132.2 Hz at the initial setting and 4.0 V and 142.6 Hz at the last follow-up, respectively. The better clinical response group (clinical improvement rate of 65–100 %) used a narrower pulse width (mean value of 78.4 μs) than the worse clinical response group (clinical improvement rate of 5–60 %, mean of value of 88.6 μs). Active contact at the GPe was used more often in the worse clinical response group than in the better response group.

Conclusions

Based on electrophysiological considerations, these patterns of stimulation parameters could be interpreted. This interpretation was based on a theoretical understanding of the mechanisms of action of DBS, i.e., that the abnormal neural signal is substituted by an induced neural signal, which is generated by therapeutic DBS.

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References

  1. Alterman RL, Miravite J, Weisz D, Shils JL, Bressman SB, Tagliati M (2007) Sixty hertz pallidal deep brain stimulation for primary torsion dystonia. Neurology 69:681–688

    Article  CAS  PubMed  Google Scholar 

  2. Alterman RL, Shils JL, Miravite J, Tagliati M (2007) Lower stimulation frequency can enhance tolerability and efficacy of pallidal deep brain stimulation for dystonia. Mov Disord 22:366–368

    Article  PubMed  Google Scholar 

  3. Anderson ME, Postupna N, Ruffo M (2003) Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. J Neurophysiol 89:1150–1160

    Article  PubMed  Google Scholar 

  4. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, Benabid AL (2000) Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience 99:289–295

    Article  CAS  PubMed  Google Scholar 

  5. Beurrier C, Bioulac B, Audin J, Hammond C (2001) High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J Neurophysiol 85:1351–1356

    CAS  PubMed  Google Scholar 

  6. Bittar RG, Yianni J, Wang S, Liu X, Nandi D, Joint C, Scott R, Bain PG, Gregory R, Stein J, Aziz TZ (2005) Deep brain stimulation for generalised dystonia and spasmodic torticollis. J Clin Neurosci 12:12–16

    Article  PubMed  Google Scholar 

  7. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci 21:1033–1038

    CAS  PubMed  Google Scholar 

  8. Butson CR, Cooper SE, Henderson JM, McIntyre CC (2007) Patient-specific analysis of the volume of tissue activated during deep brain stimulation. Neuroimage 34:661–670

    Article  PubMed  Google Scholar 

  9. Butson CR, McIntyre CC (2005) Tissue and electrode capacitance reduce neural activation volumes during deep brain stimulation. Clin Neurophysiol 116:2490–2500

    Article  PubMed  Google Scholar 

  10. Capelle HH, Blahak C, Schrader C, Baezner H, Hariz MI, Bergenheim T, Krauss JK (2012) Bilateral deep brain stimulation for cervical dystonia in patients with previous peripheral surgery. Mov Disord 27:301–304

    Article  PubMed  Google Scholar 

  11. Cheung T, Noecker AM, Alterman RL, McIntyre CC, Tagliati M (2014) Defining a therapeutic target for pallidal deep brain stimulation for dystonia. Ann Neurol 76:22–30

    Article  PubMed  Google Scholar 

  12. Cheung T, Zhang C, Rudolph J, Alterman RL, Tagliati M (2013) Sustained relief of generalized dystonia despite prolonged interruption of deep brain stimulation. Mov Disord 28:1431–1434

    Article  PubMed  Google Scholar 

  13. Chung M, Huh R (2016) Different clinical course of pallidal deep brain stimulation for phasic- and tonic-type cervical dystonia. Acta Neurochir (Wien) 158:171–180

    Article  Google Scholar 

  14. Cleary DR, Raslan AM, Rubin JE, Bahgat D, Viswanathan A, Heinricher MM, Burchiel KJ (2013) Deep brain stimulation entrains local neuronal firing in human globus pallidus internus. J Neurophysiol 109:978–987

    Article  PubMed  Google Scholar 

  15. de Hemptinne C, Ryapolova-Webb ES, Air EL, Garcia PA, Miller KJ, Ojemann JG, Ostrem JL, Galifianakis NB, Starr PA (2013) Exaggerated phase-amplitude coupling in the primary motor cortex in Parkinson disease. Proc Natl Acad Sci U S A 110:4780–4785

    Article  PubMed  PubMed Central  Google Scholar 

  16. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281–285

    Article  CAS  PubMed  Google Scholar 

  17. Eltahawy HA, Saint-Cyr J, Poon YY, Moro E, Lang AE, Lozano AM (2004) Pallidal deep brain stimulation in cervical dystonia: clinical outcome in four cases. Can J Neurol Sci 31:328–332

    Article  CAS  PubMed  Google Scholar 

  18. Garcia L, Audin J, D’Alessandro G, Bioulac B, Hammond C (2003) Dual effect of high-frequency stimulation on subthalamic neuron activity. J Neurosci 23:8743–8751

    CAS  PubMed  Google Scholar 

  19. Godinho F, Thobois S, Magnin M, Guenot M, Polo G, Benatru I, Xie J, Salvetti A, Garcia-Larrea L, Broussolle E, Mertens P (2006) Subthalamic nucleus stimulation in Parkinson’s disease: anatomical and electrophysiological localization of active contacts. J Neurol 253:1347–1355

    Article  CAS  PubMed  Google Scholar 

  20. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K (2009) Optical deconstruction of parkinsonian neural circuitry. Science 324:354–359

    Article  CAS  PubMed  Google Scholar 

  21. Grill WM Jr, Mortimer JT (1996) The effect of stimulus pulse duration on selectivity of neural stimulation. IEEE Trans Biomed Eng 43:161–166

    Article  PubMed  Google Scholar 

  22. Hammond C, Ammari R, Bioulac B, Garcia L (2008) Latest view on the mechanism of action of deep brain stimulation. Mov Disord 23:2111–2121

    Article  PubMed  Google Scholar 

  23. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23:1916–1923

    CAS  PubMed  Google Scholar 

  24. Hung SW, Hamani C, Lozano AM, Poon YY, Piboolnurak P, Miyasaki JM, Lang AE, Dostrovsky JO, Hutchison WD, Moro E (2007) Long-term outcome of bilateral pallidal deep brain stimulation for primary cervical dystonia. Neurology 68:457–459

    Article  CAS  PubMed  Google Scholar 

  25. Isaias IU, Alterman RL, Tagliati M (2008) Outcome predictors of pallidal stimulation in patients with primary dystonia: the role of disease duration. Brain 131:1895–1902

    Article  PubMed  Google Scholar 

  26. Johnson MD, Miocinovic S, McIntyre CC, Vitek JL (2008) Mechanisms and targets of deep brain stimulation in movement disorders. Neurotherapeutics 5:294–308

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kang G, Lowery MM (2014) Effects of antidromic and orthodromic activation of STN afferent axons during DBS in Parkinson’s disease: a simulation study. Front Comput Neurosci 8:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Khoo HM, Kishima H, Hosomi K, Maruo T, Tani N, Oshino S, Shimokawa T, Yokoe M, Mochizuki H, Saitoh Y, Yoshimine T (2014) Low-frequency subthalamic nucleus stimulation in Parkinson’s disease: a randomized clinical trial. Mov Disord 29:270–274

    Article  PubMed  Google Scholar 

  29. Kiss ZH, Doig-Beyaert K, Eliasziw M, Tsui J, Haffenden A, Suchowersky O (2007) The Canadian multicentre study of deep brain stimulation for cervical dystonia. Brain 130:2879–2886

    Article  PubMed  Google Scholar 

  30. Krauss JK (2010) Surgical treatment of dystonia. Eur J Neurol 17(Suppl 1):97–101

    Article  PubMed  Google Scholar 

  31. Krauss JK, Loher TJ, Pohle T, Weber S, Taub E, Barlocher CB, Burgunder JM (2002) Pallidal deep brain stimulation in patients with cervical dystonia and severe cervical dyskinesias with cervical myelopathy. J Neurol Neurosurg Psychiatry 72:249–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kuhn AA, Brandt SA, Kupsch A, Trottenberg T, Brocke J, Irlbacher K, Schneider GH, Meyer BU (2004) Comparison of motor effects following subcortical electrical stimulation through electrodes in the globus pallidus internus and cortical transcranial magnetic stimulation. Exp Brain Res 155:48–55

    Article  PubMed  Google Scholar 

  33. Kuncel AM, Grill WM (2004) Selection of stimulus parameters for deep brain stimulation. Clin Neurophysiol 115:2431–2441

    Article  PubMed  Google Scholar 

  34. Li Q, Ke Y, Chan DC, Qian ZM, Yung KK, Ko H, Arbuthnott GW, Yung WH (2012) Therapeutic deep brain stimulation in Parkinsonian rats directly influences motor cortex. Neuron 76:1030–1041

    Article  CAS  PubMed  Google Scholar 

  35. Li Q, Qian ZM, Arbuthnott GW, Ke Y, Yung WH (2014) Cortical effects of deep brain stimulation: implications for pathogenesis and treatment of Parkinson disease. JAMA Neurol 71:100–103

    Article  PubMed  Google Scholar 

  36. Lozano AM, Lipsman N (2013) Probing and regulating dysfunctional circuits using deep brain stimulation. Neuron 77:406–424

    Article  CAS  PubMed  Google Scholar 

  37. McIntyre CC, Savasta M, Walter BL, Vitek JL (2004) How does deep brain stimulation work? Present understanding and future questions. J Clin Neurophysiol 21:40–50

    Article  PubMed  Google Scholar 

  38. Miocinovic S, Lempka SF, Russo GS, Maks CB, Butson CR, Sakaie KE, Vitek JL, McIntyre CC (2009) Experimental and theoretical characterization of the voltage distribution generated by deep brain stimulation. Exp Neurol 216:166–176

    Article  PubMed  Google Scholar 

  39. Molnar G, Barolat G (2014) Principles of cord activation during spinal cord stimulation. Neuromodulation 17(Suppl 1):12–21

    Article  PubMed  Google Scholar 

  40. Montgomery EB Jr (2006) Effects of GPi stimulation on human thalamic neuronal activity. Clin Neurophysiol 117:2691–2702

    Article  PubMed  Google Scholar 

  41. Moro E, Esselink RJ, Xie J, Hommel M, Benabid AL, Pollak P (2002) The impact on Parkinson’s disease of electrical parameter settings in STN stimulation. Neurology 59:706–713

    Article  CAS  PubMed  Google Scholar 

  42. Ostrem JL, Starr PA (2008) Treatment of dystonia with deep brain stimulation. Neurotherapeutics 5:320–330

    Article  PubMed  Google Scholar 

  43. Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20:91–127

    Article  CAS  PubMed  Google Scholar 

  44. Parent M, Parent A (2004) The pallidofugal motor fiber system in primates. Parkinsonism Relat Disord 10:203–211

    Article  PubMed  Google Scholar 

  45. Plaha P, Ben-Shlomo Y, Patel NK, Gill SS (2006) Stimulation of the caudal zona incerta is superior to stimulation of the subthalamic nucleus in improving contralateral parkinsonism. Brain 129:1732–1747

    Article  PubMed  Google Scholar 

  46. Pretto TE, Dalvi A, Kang UJ, Penn RD (2008) A prospective blinded evaluation of deep brain stimulation for the treatment of secondary dystonia and primary torticollis syndromes. J Neurosurg 109:405–409

    Article  PubMed  Google Scholar 

  47. Ranck JB Jr (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440

    Article  PubMed  Google Scholar 

  48. Rattay F (1999) The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 89:335–346

    Article  CAS  PubMed  Google Scholar 

  49. Saint-Cyr JA, Hoque T, Pereira LC, Dostrovsky JO, Hutchison WD, Mikulis DJ, Abosch A, Sime E, Lang AE, Lozano AM (2002) Localization of clinically effective stimulating electrodes in the human subthalamic nucleus on magnetic resonance imaging. J Neurosurg 97:1152–1166

    Article  PubMed  Google Scholar 

  50. Schaltenbrand G, Wahren W, Hassler R (1977) Atlas for stereotaxy of the human brain. Thieme Rüdigerstraße 14, D-70469 Stuttgart

  51. Skogseid IM (2014) Dystonia–new advances in classification, genetics, pathophysiology and treatment. Acta Neurol Scand Suppl:13–19

  52. Starr PA, Turner RS, Rau G, Lindsey N, Heath S, Volz M, Ostrem JL, Marks WJ Jr (2006) Microelectrode-guided implantation of deep brain stimulators into the globus pallidus internus for dystonia: techniques, electrode locations, and outcomes. J Neurosurg 104:488–501

    Article  PubMed  Google Scholar 

  53. Tisch S, Zrinzo L, Limousin P, Bhatia KP, Quinn N, Ashkan K, Hariz M (2007) Effect of electrode contact location on clinical efficacy of pallidal deep brain stimulation in primary generalised dystonia. J Neurol Neurosurg Psychiatry 78:1314–1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Tolleson C, Pallavaram S, Li C, Fang J, Phibbs F, Konrad P, Hedera P, D’Haese PF, Dawant BM, Davis TL (2015) The optimal pallidal target in deep brain stimulation for dystonia: a study using a functional atlas based on nonlinear image registration. Stereotact Funct Neurosurg 93:17–24

    Article  PubMed  Google Scholar 

  55. Udupa K, Chen R (2015) The mechanisms of action of deep brain stimulation and ideas for the future development. Prog Neurobiol 133:27–49

    Article  PubMed  Google Scholar 

  56. Vallabhajosula S, Haq IU, Hwynn N, Oyama G, Okun M, Tillman MD, Hass CJ (2015) Low-frequency versus high-frequency subthalamic nucleus deep brain stimulation on postural control and gait in Parkinson’s disease: a quantitative study. Brain Stimul 8:64–75

    Article  PubMed  Google Scholar 

  57. Vercueil L, Houeto JL, Krystkowiak P, Lagrange C, Cassim F, Benazzouz A, Pidoux B, Destee A, Agid Y, Cornu P, Blond S, Benabid AL, Pollak P, Vidailhet M (2007) Effects of pulse width variations in pallidal stimulation for primary generalized dystonia. J Neurol 254:1533–1537

    Article  PubMed  Google Scholar 

  58. Wei XF, Grill WM (2009) Impedance characteristics of deep brain stimulation electrodes in vitro and in vivo. J Neural Eng 6:046008

    Article  PubMed  PubMed Central  Google Scholar 

  59. Weinberger M, Hutchison WD, Alavi M, Hodaie M, Lozano AM, Moro E, Dostrovsky JO (2012) Oscillatory activity in the globus pallidus internus: comparison between Parkinson’s disease and dystonia. Clin Neurophysiol 123:358–368

    Article  PubMed  Google Scholar 

  60. Windels F, Bruet N, Poupard A, Feuerstein C, Bertrand A, Savasta M (2003) Influence of the frequency parameter on extracellular glutamate and gamma-aminobutyric acid in substantia nigra and globus pallidus during electrical stimulation of subthalamic nucleus in rats. J Neurosci Res 72:259–267

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Neurosurgery, Incheon St. Mary’s Hospital, The Catholic University of Korea, Incheon, South Korea

    Ryoong Huh

  2. Department of Neurosurgery, Soonchunhyang University Bucheon Hospital, 170 Jomaru-ro, Wonmi-gu, Bucheon-city, Gyeonggi-do, South Korea

    Moonyoung Chung

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  1. Ryoong Huh
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  2. Moonyoung Chung
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Correspondence to Moonyoung Chung.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Additional information

Some data in this study were orally presented in the 10th Scientific meeting for the Asian Australasian Society of Stereotactic and Functional Neurosurgery in Shangri-La Hotel, Cairns, Australia on 3–5 March, 2016.

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Huh, R., Chung, M. Electrophysiological interpretations of the clinical response to stimulation parameters of pallidal deep brain stimulation for cervical dystonia. Acta Neurochir 158, 2029–2038 (2016). https://doi.org/10.1007/s00701-016-2942-x

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  • DOI: https://doi.org/10.1007/s00701-016-2942-x

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