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Published in: Experimental Brain Research 1/2013

01-05-2013 | Research Article

The impact of low-frequency stimulation of subthalamic region on self-generated isometric contraction in patients with Parkinson’s disease

Authors: Chiung Chu Chen, Wey Yil Lin, Hsiao Lung Chan, Po Hsun Tu, Shih Tseng Lee, Chin Song Lu, Peter Brown

Published in: Experimental Brain Research | Issue 1/2013

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Abstract

Growing evidence suggests that spontaneous oscillatory low-frequency synchronization in the subthalamic nuclei (STN) may modulate motor performance in patients with Parkinson’s disease (PD). To explore this in more detail, 15 PD patients chronically implanted with deep brain stimulation (DBS) electrodes in both STN were stimulated bilaterally at 5, 10, 20, 50 and 130 Hz and the effects of the DBS on self-initiated isometric elbow flexion (FLEX) and finger pinch (PINCH) were compared to performance without DBS. Baseline performance was very much impaired. Peak force was significantly greater during 130 and 10 Hz stimulation when compared to no stimulation in both tasks. Cumulative sums of the changes in mean rising force and peak force in the two tasks upon stimulation at 10 and 20 Hz demonstrated that patients improved their performance on stimulation, except for those with the best performance off stimulation who deteriorated with stimulation at 20 Hz. Thus, no effect was detected with 20 Hz stimulation at the group level. The current study highlights the need to consider the baseline performance of a subject in a given task when determining the effects of low-frequency STN stimulation in PD patients. It also demonstrates that stimulation at 10 Hz can improve motor function in subjects with poor baseline function.
Literature
go back to reference Anzak A, Tan H, Pogosyan A, Foltynie T, Limousin P, Zrinzo L, Hariz M, Ashkan K, Bogdanovic M, Green AL, Aziz T, Brown P (2012) Subthalamic nucleus activity optimizes maximal effort motor responses in Parkinson’s disease. Brain 135:2766–2778PubMedCrossRef Anzak A, Tan H, Pogosyan A, Foltynie T, Limousin P, Zrinzo L, Hariz M, Ashkan K, Bogdanovic M, Green AL, Aziz T, Brown P (2012) Subthalamic nucleus activity optimizes maximal effort motor responses in Parkinson’s disease. Brain 135:2766–2778PubMedCrossRef
go back to reference Brown P, Chen CC, Wang S, Kuhn AA, Doyle L, Yarrow K, Nuttin B, Stein J, Aziz T (2006) Involvement of human basal ganglia in off-line feed-back control of voluntary movement. Curr Biol 16:2129–2134PubMedCrossRef Brown P, Chen CC, Wang S, Kuhn AA, Doyle L, Yarrow K, Nuttin B, Stein J, Aziz T (2006) Involvement of human basal ganglia in off-line feed-back control of voluntary movement. Curr Biol 16:2129–2134PubMedCrossRef
go back to reference Chen CC, Lee ST, Wu T, Chen CJ, Chen MC, Lu CS (2003) Short-term effect of bilateral subthalamic stimulation for advanced Parkinson’s disease. Chang Gung Med J 26:322–351 Chen CC, Lee ST, Wu T, Chen CJ, Chen MC, Lu CS (2003) Short-term effect of bilateral subthalamic stimulation for advanced Parkinson’s disease. Chang Gung Med J 26:322–351
go back to reference Chen CC, Brucke C, Kempf F, Kupsch A, Lu CS, Lee ST, Tisch S, Limousin P, Hariz M, Brown P (2006) Deep brain stimulation of the subthalamic nucleus: a two-edged sword. Curr Biol 16:R952–R953PubMedCrossRef Chen CC, Brucke C, Kempf F, Kupsch A, Lu CS, Lee ST, Tisch S, Limousin P, Hariz M, Brown P (2006) Deep brain stimulation of the subthalamic nucleus: a two-edged sword. Curr Biol 16:R952–R953PubMedCrossRef
go back to reference Chen CC, Litvak V, Gilbertson T, Kuhn AA, Lu CS, Lee ST, Tsai CH, Tisch S, Limousin P, Hariz M, Brown P (2007) Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson’s disease. Exp Neurol 231:91–96CrossRef Chen CC, Litvak V, Gilbertson T, Kuhn AA, Lu CS, Lee ST, Tsai CH, Tisch S, Limousin P, Hariz M, Brown P (2007) Excessive synchronization of basal ganglia neurons at 20 Hz slows movement in Parkinson’s disease. Exp Neurol 231:91–96CrossRef
go back to reference Chen CC, Hsu YT, Chan HL, Chiou SM, Tu PH, Lee ST, Tsai CH, Lu CS, Brown P (2010) Complexity of subthalamic 13–35 Hz oscillatory activity directly correlates with clinical impairment in patients with Parkinson’s disease. Exp Neurol 224:234–240PubMedCrossRef Chen CC, Hsu YT, Chan HL, Chiou SM, Tu PH, Lee ST, Tsai CH, Lu CS, Brown P (2010) Complexity of subthalamic 13–35 Hz oscillatory activity directly correlates with clinical impairment in patients with Parkinson’s disease. Exp Neurol 224:234–240PubMedCrossRef
go back to reference Chen CC, Lin WY, Chan HL, Hsu YT, Tu PH, Lee ST, Chiou SM, Tsai CH, Lu CS, Brown P (2011) Stimulation of the subthalamic region at 20 Hz slows the development of grip force in Parkinson’s disease. Exp Neurol 231:91–96PubMedCrossRef Chen CC, Lin WY, Chan HL, Hsu YT, Tu PH, Lee ST, Chiou SM, Tsai CH, Lu CS, Brown P (2011) Stimulation of the subthalamic region at 20 Hz slows the development of grip force in Parkinson’s disease. Exp Neurol 231:91–96PubMedCrossRef
go back to reference Curran-Everett D (2000) Multiple comparisons: philosophies and illustrations. Am J Physiol Regul Integr Comp Physiol 279:1–8 Curran-Everett D (2000) Multiple comparisons: philosophies and illustrations. Am J Physiol Regul Integr Comp Physiol 279:1–8
go back to reference Eusebio A, Chen CC, Lu CS, Lee ST, Tsai CH, Limousin P, Hariz M, Brown P (2008) Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson’s disease. Exp Neurol 209:125–130PubMedCrossRef Eusebio A, Chen CC, Lu CS, Lee ST, Tsai CH, Limousin P, Hariz M, Brown P (2008) Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson’s disease. Exp Neurol 209:125–130PubMedCrossRef
go back to reference Eusebio A, Pogosyan A, Wang S, Averbeck B, Gaynor LD, Cantiniaux S, Witjas T, Limousin P, Azulay JP, Brown P (2009) Resonance in subthalamo-cortical circuits in Parkinson’s disease. Brain 132:2139–2150PubMedCrossRef Eusebio A, Pogosyan A, Wang S, Averbeck B, Gaynor LD, Cantiniaux S, Witjas T, Limousin P, Azulay JP, Brown P (2009) Resonance in subthalamo-cortical circuits in Parkinson’s disease. Brain 132:2139–2150PubMedCrossRef
go back to reference Fogelson N, Williams D, Tijssen M, van Bruggen G, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the subthalamic area in Parkinson’s disease. Cereb Cortex 16:64–75PubMedCrossRef Fogelson N, Williams D, Tijssen M, van Bruggen G, Speelman H, Brown P (2006) Different functional loops between cerebral cortex and the subthalamic area in Parkinson’s disease. Cereb Cortex 16:64–75PubMedCrossRef
go back to reference Hirschmann J, Özkurt TE, Butz M, Homburger M, Elben S, Hartmann CJ, Vesper J, Wojtecki L, Schnitzler A (2011) Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson’s disease. NeuroImage 55:1159–1168PubMedCrossRef Hirschmann J, Özkurt TE, Butz M, Homburger M, Elben S, Hartmann CJ, Vesper J, Wojtecki L, Schnitzler A (2011) Distinct oscillatory STN-cortical loops revealed by simultaneous MEG and local field potential recordings in patients with Parkinson’s disease. NeuroImage 55:1159–1168PubMedCrossRef
go back to reference Jenkinson N, Brown P (2011) New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci 34:611–618PubMedCrossRef Jenkinson N, Brown P (2011) New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci 34:611–618PubMedCrossRef
go back to reference Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Benabid AL, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934PubMedCrossRef Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Benabid AL, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934PubMedCrossRef
go back to reference Livtak V, Jha A, Eusebio A, Oostenveld R, Foltynie T, Limousin P, Zrinzo L, Hariz MI, Friston K, Brown P (2011) Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson’s disease. Brain 134:359–374CrossRef Livtak V, Jha A, Eusebio A, Oostenveld R, Foltynie T, Limousin P, Zrinzo L, Hariz MI, Friston K, Brown P (2011) Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson’s disease. Brain 134:359–374CrossRef
go back to reference Lopez-Azcarate J, Tainta M, Rodriguez-Oroz MC, Valencia M, Gonzalez R, Guridi J, Iriarte J, Obeso JA, Artieda J, Alegre M (2010) Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson’s disease. J Neurosci 12:6667–6677CrossRef Lopez-Azcarate J, Tainta M, Rodriguez-Oroz MC, Valencia M, Gonzalez R, Guridi J, Iriarte J, Obeso JA, Artieda J, Alegre M (2010) Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson’s disease. J Neurosci 12:6667–6677CrossRef
go back to reference 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 59:706–713PubMedCrossRef 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 59:706–713PubMedCrossRef
go back to reference Ray NJ, Jenkinson N, Wang S, Holland P, Brittain JS, Joint C, Stein JF, Aziz T (2008) Local field potential beta activity in the subthalamic nucleus of patients with Parkinson’s disease is associated with improvement in bradykinesia after dopamine and deep brain stimulation. Exp Neurol 213:108–113PubMedCrossRef Ray NJ, Jenkinson N, Wang S, Holland P, Brittain JS, Joint C, Stein JF, Aziz T (2008) Local field potential beta activity in the subthalamic nucleus of patients with Parkinson’s disease is associated with improvement in bradykinesia after dopamine and deep brain stimulation. Exp Neurol 213:108–113PubMedCrossRef
go back to reference Ray NJ, Jenkinson N, Brittan J, Holland P, Joint C, Nandi D, Bain PG, Yousif N, Green A, Stein JS, Aziz TZ (2009) The role of the subthalamic nucleus in response inhibition: evidence from deep brain stimulation for Parkinson’s disease. Neuropsychologia 47:2828–2834PubMedCrossRef Ray NJ, Jenkinson N, Brittan J, Holland P, Joint C, Nandi D, Bain PG, Yousif N, Green A, Stein JS, Aziz TZ (2009) The role of the subthalamic nucleus in response inhibition: evidence from deep brain stimulation for Parkinson’s disease. Neuropsychologia 47:2828–2834PubMedCrossRef
go back to reference Pogosyan A, Yoshida F, Chen CC, Martinez-Torres I, Foltynie T, Limousin P, Zrinzo L, Hariz MI, Brown P (2010) Parkinsonian impairment correlates with spatially extensive subthalamic oscillatory synchronization. Neuroscience 24:245–257CrossRef Pogosyan A, Yoshida F, Chen CC, Martinez-Torres I, Foltynie T, Limousin P, Zrinzo L, Hariz MI, Brown P (2010) Parkinsonian impairment correlates with spatially extensive subthalamic oscillatory synchronization. Neuroscience 24:245–257CrossRef
go back to reference Singh A, Levin J, Mehrkens JH, Botzel K (2011) Alpha frequency modulation in the human basal ganglia is dependent on motor task. Eur J Neurosci 33:960–967PubMedCrossRef Singh A, Levin J, Mehrkens JH, Botzel K (2011) Alpha frequency modulation in the human basal ganglia is dependent on motor task. Eur J Neurosci 33:960–967PubMedCrossRef
go back to reference Tan H, Pogosyan A, Anzak A, Foltynie T, Limousin P, Zrinzo L, Ashkan K, Bogdanovic M, Green AL, Aziz T, Brown P (2013) Frequency specific activity in subthalamic nucleus correlates with hand bradykinesia in Parkinson’s disease. Exp Neurol 240:122–129PubMedCrossRef Tan H, Pogosyan A, Anzak A, Foltynie T, Limousin P, Zrinzo L, Ashkan K, Bogdanovic M, Green AL, Aziz T, Brown P (2013) Frequency specific activity in subthalamic nucleus correlates with hand bradykinesia in Parkinson’s disease. Exp Neurol 240:122–129PubMedCrossRef
go back to reference Temperli P, Ghika J, Villemure JG, Burkhard PR, Bogousslavsky J, Vingerhoets FJ (2003) How do parkinsonian signs return after discontinuation of subthalamic DBS? Neurology 14:78–81CrossRef Temperli P, Ghika J, Villemure JG, Burkhard PR, Bogousslavsky J, Vingerhoets FJ (2003) How do parkinsonian signs return after discontinuation of subthalamic DBS? Neurology 14:78–81CrossRef
go back to reference Timmermann L, Wojtecki L, Gross J, Lehrke R, Voges J, Maarouf M, Treuer H, Sturm V, Schnitzler A (2004) Ten-Hertz stimulation of subthalamic nucleus deteriorates motor symptoms in Parkinson’s disease. Mov Disord 19:1328–1333PubMedCrossRef Timmermann L, Wojtecki L, Gross J, Lehrke R, Voges J, Maarouf M, Treuer H, Sturm V, Schnitzler A (2004) Ten-Hertz stimulation of subthalamic nucleus deteriorates motor symptoms in Parkinson’s disease. Mov Disord 19:1328–1333PubMedCrossRef
go back to reference Tsang EW, Hamani C, Moro E, Mazzella F, Saha U, Lozano AM, Hodaie M, Chuang R, Steeves T, Lim SY, Neagu B, Chen R (2012) Subthalamic deep brain stimulation at individualized frequencies for Parkinson’s disease. Neurology 78:1930–1938PubMedCrossRef Tsang EW, Hamani C, Moro E, Mazzella F, Saha U, Lozano AM, Hodaie M, Chuang R, Steeves T, Lim SY, Neagu B, Chen R (2012) Subthalamic deep brain stimulation at individualized frequencies for Parkinson’s disease. Neurology 78:1930–1938PubMedCrossRef
go back to reference Wojtecki L, Timmermann L, Jorgens S, Sudmeyer M, Maarouf M, Treuer H, Gross J, Lehrke R, Koulousakis A, Voges J, Sturm V, Schnitzler A (2006) Frequency-dependent reciprocal modulation of verbal fluency and motor functions in subthalamic deep brain stimulation. Arch Neurol 63:1273–1276PubMedCrossRef Wojtecki L, Timmermann L, Jorgens S, Sudmeyer M, Maarouf M, Treuer H, Gross J, Lehrke R, Koulousakis A, Voges J, Sturm V, Schnitzler A (2006) Frequency-dependent reciprocal modulation of verbal fluency and motor functions in subthalamic deep brain stimulation. Arch Neurol 63:1273–1276PubMedCrossRef
Metadata
Title
The impact of low-frequency stimulation of subthalamic region on self-generated isometric contraction in patients with Parkinson’s disease
Authors
Chiung Chu Chen
Wey Yil Lin
Hsiao Lung Chan
Po Hsun Tu
Shih Tseng Lee
Chin Song Lu
Peter Brown
Publication date
01-05-2013
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2013
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-013-3484-6

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