Skip to main content
Top
Published in: Journal of Neurology 2/2021

01-02-2021 | Deep Brain Stimulation | Original Communication

Deep brain stimulation of the internal globus pallidus does not affect the limbic circuit in patients with Parkinson’s disease: a PET study

Authors: Xavier Palard-Novello, Sophie Drapier, Alexandre Bonnet, Antoine Girard, Gabriel Robert, Jean-François Houvenaghel, Paul Sauleau, Marc Vérin, Claire Haegelen, Florence Le Jeune

Published in: Journal of Neurology | Issue 2/2021

Login to get access

Abstract

Introduction

Internal globus pallidus (GPi) deep brain stimulation (DBS) is a safe and effective alternative treatment in Parkinson’s disease (PD) for patients with cognitive impairment. However, no study has yet investigated metabolic changes within a large series of patients undergoing GPi stimulation.

Objective

We assessed motor, cognitive and psychiatric changes, as well as modifications in brain glucose metabolism measured with FDG-PET, before and after bilateral GPi-DBS.

Methods

In the same week, 32 patients with PD underwent a motor, cognitive and psychiatric assessment and a resting-state FDG-PET scan, 4 months before and 4 months after GPi-DBS surgery. For the voxelwise metabolic change assessment, the p value was controlled for multiple comparisons using the family wise error rate.

Results

After GPi-DBS surgery, patients showed a significant overall improvement in motor status. No cognitive or psychiatric changes were observed after surgery. Nor were any clusters with significantly relative metabolic changes found in the limbic circuit after surgery. Clusters with significantly relative metabolic changes were observed in the left and right Brodmann area (BA) 6, the right BA 9, the right and left BA 39 and the left BA 17.

Conclusion

The present study confirmed that GPi-DBS is an effective treatment in patients with advanced PD, owing to metabolic changes in the areas involved in motor execution. The absence of relative metabolic decrease in the limbic circuit and the few changes affecting the associative circuit could explain why GPi-DBS is cognitively safe.
Literature
1.
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, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934CrossRef Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, Koudsie A, Limousin PD, Benazzouz A, LeBas JF, Pollak P (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934CrossRef
2.
go back to reference Parsons TD, Rogers SA, Braaten AJ, Woods SP, Troster AI (2006) Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol 5:578–588CrossRef Parsons TD, Rogers SA, Braaten AJ, Woods SP, Troster AI (2006) Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol 5:578–588CrossRef
3.
go back to reference Volkmann J, Allert N, Voges J, Weiss PH, Freund HJ, Sturm V (2001) Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD. Neurology 56:548–551CrossRef Volkmann J, Allert N, Voges J, Weiss PH, Freund HJ, Sturm V (2001) Safety and efficacy of pallidal or subthalamic nucleus stimulation in advanced PD. Neurology 56:548–551CrossRef
4.
go back to reference Allert N, Volkmann J, Dotse S, Hefter H, Sturm V, Freund HJ (2001) Effects of bilateral pallidal or subthalamic stimulation on gait in advanced Parkinson’s disease. Mov Dis 16:1076–1085CrossRef Allert N, Volkmann J, Dotse S, Hefter H, Sturm V, Freund HJ (2001) Effects of bilateral pallidal or subthalamic stimulation on gait in advanced Parkinson’s disease. Mov Dis 16:1076–1085CrossRef
5.
go back to reference Drapier D, Drapier S, Sauleau P, Haegelen C, Raoul S, Biseul I, Peron J, Lallement F, Reymann JM, Edan G, Verin M, Millet B (2006) Does subthalamic nucleus stimulation induce apathy in Parkinson’s disease? J Neurol 253:1083–1091CrossRef Drapier D, Drapier S, Sauleau P, Haegelen C, Raoul S, Biseul I, Peron J, Lallement F, Reymann JM, Edan G, Verin M, Millet B (2006) Does subthalamic nucleus stimulation induce apathy in Parkinson’s disease? J Neurol 253:1083–1091CrossRef
6.
go back to reference Funkiewiez A, Ardouin C, Caputo E, Krack P, Fraix V, Klinger H, Chabardes S, Foote K, Benbid AL, Pollak P (2004) Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:834–839CrossRef Funkiewiez A, Ardouin C, Caputo E, Krack P, Fraix V, Klinger H, Chabardes S, Foote K, Benbid AL, Pollak P (2004) Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:834–839CrossRef
7.
go back to reference Bonenfant J, Drapier S, Houvenaghel JF, Naudet F, Haegelen C, Sauleau P, Vérin M (2017) Pallidal stimulation in Parkinson’s patients with contraindications to subthalamic target: a 3 years follow-up. Parkinsonism Relat Disord 34:20–25CrossRef Bonenfant J, Drapier S, Houvenaghel JF, Naudet F, Haegelen C, Sauleau P, Vérin M (2017) Pallidal stimulation in Parkinson’s patients with contraindications to subthalamic target: a 3 years follow-up. Parkinsonism Relat Disord 34:20–25CrossRef
8.
go back to reference Lachenmayer ML, Bettschen C, Bernasconi C, Petermann K, Debove I, Muellner J, Michelis JP, Burgunder JM, Krauss JK, Ortel MF, Pollo C, Kaelin-Lang A, Schüpbach M (2019) Stimulation of the globus pallidus internus in the treatment of Parkinson’s disease: long-term results of a monocentric cohort. Parkinsonism Relat Disord 64:118–123CrossRef Lachenmayer ML, Bettschen C, Bernasconi C, Petermann K, Debove I, Muellner J, Michelis JP, Burgunder JM, Krauss JK, Ortel MF, Pollo C, Kaelin-Lang A, Schüpbach M (2019) Stimulation of the globus pallidus internus in the treatment of Parkinson’s disease: long-term results of a monocentric cohort. Parkinsonism Relat Disord 64:118–123CrossRef
9.
go back to reference Lozachmeur C, Drapier S, Robert G, Dondaine T, Laviolle B, Sauleau P, Peron J, Le Jeune F, Travers D, Millet B, Vérin M, Drapier D (2014) Pallidal stimulation in Parkinson’s disease does not induce apathy. J Neuropsychiatry Clin Neurosci 26:221–226CrossRef Lozachmeur C, Drapier S, Robert G, Dondaine T, Laviolle B, Sauleau P, Peron J, Le Jeune F, Travers D, Millet B, Vérin M, Drapier D (2014) Pallidal stimulation in Parkinson’s disease does not induce apathy. J Neuropsychiatry Clin Neurosci 26:221–226CrossRef
10.
go back to reference Rouaud T, Dondaine T, Drapier S, Haegelen C, Lallement F, Peron J, Raoul S, Sauleau P, Vérin M (2010) Pallidal stimulation in advanced Parkinson’s patients with contraindications for subthalamic stimulation. Mov Disord 25:1839–1846CrossRef Rouaud T, Dondaine T, Drapier S, Haegelen C, Lallement F, Peron J, Raoul S, Sauleau P, Vérin M (2010) Pallidal stimulation in advanced Parkinson’s patients with contraindications for subthalamic stimulation. Mov Disord 25:1839–1846CrossRef
11.
go back to reference Le Jeune F, Drapier D, Bourguignon A, Peron J, Mesbah H, Drapier S, Sauleau P, Haegelen C, Travers D, Garin E, Malbert CH, Millet B, Vérin M (2009) Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study. Neurology 73:1746–1751CrossRef Le Jeune F, Drapier D, Bourguignon A, Peron J, Mesbah H, Drapier S, Sauleau P, Haegelen C, Travers D, Garin E, Malbert CH, Millet B, Vérin M (2009) Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study. Neurology 73:1746–1751CrossRef
12.
go back to reference Le Jeune F, Peron J, Biseul I, Fournier S, Sauleau P, Drapier S, Haegelen C, Drapier D, Millet B, Garin E, Herry JH, Malbert CH, Vérin M (2008) Subthalamic nucleus stimulation affects orbitofrontal cortex in facial emotion recognition: a PET study. Brain 131:1599–1608CrossRef Le Jeune F, Peron J, Biseul I, Fournier S, Sauleau P, Drapier S, Haegelen C, Drapier D, Millet B, Garin E, Herry JH, Malbert CH, Vérin M (2008) Subthalamic nucleus stimulation affects orbitofrontal cortex in facial emotion recognition: a PET study. Brain 131:1599–1608CrossRef
13.
go back to reference Le Jeune F, Peron J, Grandjean D, Drapier S, Haegelen C, Garin E, Millet B, Vérin M (2010) Subthalamic nucleus stimulation affects limbic and associative circuits: a PET study. Eur J Nucl Med Mol Imaging 37:1512–1520CrossRef Le Jeune F, Peron J, Grandjean D, Drapier S, Haegelen C, Garin E, Millet B, Vérin M (2010) Subthalamic nucleus stimulation affects limbic and associative circuits: a PET study. Eur J Nucl Med Mol Imaging 37:1512–1520CrossRef
14.
go back to reference Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752CrossRef Gibb WR, Lees AJ (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson’s disease. J Neurol Neurosurg Psychiatry 51:745–752CrossRef
15.
go back to reference Silberstein P, Bittar RG, Boyle R, Cook R, Coyne T, O'Sullivan D, Pell M, Peppard R, Rodrigues J, Silburn P, Stell R, Watson P (2009) Deep brain stimulation for Parkinson’s disease: Australian referral guidelines. J Clin Neurosci 16:1001–1008CrossRef Silberstein P, Bittar RG, Boyle R, Cook R, Coyne T, O'Sullivan D, Pell M, Peppard R, Rodrigues J, Silburn P, Stell R, Watson P (2009) Deep brain stimulation for Parkinson’s disease: Australian referral guidelines. J Clin Neurosci 16:1001–1008CrossRef
16.
go back to reference Welter ML, Houeto JL, du Montcel ST, Mesnage V, Bonnet AM, Pillon B, Arnulf I, Pidoux B, Dormont D, Cornu P, Agid Y (2002) Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 125:575–583CrossRef Welter ML, Houeto JL, du Montcel ST, Mesnage V, Bonnet AM, Pillon B, Arnulf I, Pidoux B, Dormont D, Cornu P, Agid Y (2002) Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 125:575–583CrossRef
17.
go back to reference Fahn S, Elton R, UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne DB, et al. (eds) Recent developments in Parkinson’s disease. Macmillan, Florham Park, pp 153–163 Fahn S, Elton R, UPDRS Development Committee (1987) Unified Parkinson’s disease rating scale. In: Fahn S, Marsden CD, Calne DB, et al. (eds) Recent developments in Parkinson’s disease. Macmillan, Florham Park, pp 153–163
18.
go back to reference Varrone A, Asenbaum S, Vander Borght T, Booij J, Nobili F, Nagren K, Darcourt J, Kapucu OL, Tatsch K, Bartenstein P, van Laere K, European Association of Nuclear Medicine Neuroimaging Committee (2009) EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2. Eur J Nucl Med Mol Imaging 36:2103–2110CrossRef Varrone A, Asenbaum S, Vander Borght T, Booij J, Nobili F, Nagren K, Darcourt J, Kapucu OL, Tatsch K, Bartenstein P, van Laere K, European Association of Nuclear Medicine Neuroimaging Committee (2009) EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2. Eur J Nucl Med Mol Imaging 36:2103–2110CrossRef
19.
go back to reference Meles SK, Renken RJ, Pagani M, Teune LK, Arnaldi D, Morbelli S, Nobili F, van Laar T, Obeso JA, Rodriguez-Oroz MC, Leenders KL (2020) Abnormal pattern of brain glucose metabolism in Parkinson’s disease: replication in three European cohorts. Eur J Nucl Med Mol Imaging 47:437–450CrossRef Meles SK, Renken RJ, Pagani M, Teune LK, Arnaldi D, Morbelli S, Nobili F, van Laar T, Obeso JA, Rodriguez-Oroz MC, Leenders KL (2020) Abnormal pattern of brain glucose metabolism in Parkinson’s disease: replication in three European cohorts. Eur J Nucl Med Mol Imaging 47:437–450CrossRef
20.
go back to reference Asanuma K, Tang C, Ma Y, Dhawan V, Mattis P, Edwards C, Kaplitt MG, Feigin A, Eidelberg D (2006) Network modulation in the treatment of Parkinson’s disease. Brain 129:2667–2678CrossRef Asanuma K, Tang C, Ma Y, Dhawan V, Mattis P, Edwards C, Kaplitt MG, Feigin A, Eidelberg D (2006) Network modulation in the treatment of Parkinson’s disease. Brain 129:2667–2678CrossRef
21.
go back to reference Geday J, Ostergaard K, Johnsen E, Gjedde A (2009) STN stimulation in Parkinson’s disease restores striatal inhibition of thalamocortical projection. Hum Brain Mapp 30:112–121CrossRef Geday J, Ostergaard K, Johnsen E, Gjedde A (2009) STN stimulation in Parkinson’s disease restores striatal inhibition of thalamocortical projection. Hum Brain Mapp 30:112–121CrossRef
22.
go back to reference Hershey T, Revilla FJ, Wernle AR, McGee-Minnich L, Antenor JV, Videen TO, Dowling JL, Mink JW, Perlmutter JS (2003) Cortical and subcortical blood flow effects of subthalamic nucleus stimulation in PD. Neurology 61:816–821CrossRef Hershey T, Revilla FJ, Wernle AR, McGee-Minnich L, Antenor JV, Videen TO, Dowling JL, Mink JW, Perlmutter JS (2003) Cortical and subcortical blood flow effects of subthalamic nucleus stimulation in PD. Neurology 61:816–821CrossRef
23.
go back to reference Trost M, Su S, Su P, Yen RF, Tseng HM, Barnes A, Ma Y, Eidelberg D (2006) Network modulation by the subthalamic nucleus in the treatment of Parkinson’s disease. Neuroimage 31:301–307CrossRef Trost M, Su S, Su P, Yen RF, Tseng HM, Barnes A, Ma Y, Eidelberg D (2006) Network modulation by the subthalamic nucleus in the treatment of Parkinson’s disease. Neuroimage 31:301–307CrossRef
24.
go back to reference Fukuda M, Mentis MJ, Ma Y, Dhawan V, Antonini A, Lang AE, Lozano AM, Hammerstad J, Lyons K, Koller WC, Moeller JR, Eidelberg D (2001) Networks mediating the clinical effects of pallidal brain stimulation for Parkinson’s disease: a PET study of resting-state glucose metabolism. Brain 124:1601–1609CrossRef Fukuda M, Mentis MJ, Ma Y, Dhawan V, Antonini A, Lang AE, Lozano AM, Hammerstad J, Lyons K, Koller WC, Moeller JR, Eidelberg D (2001) Networks mediating the clinical effects of pallidal brain stimulation for Parkinson’s disease: a PET study of resting-state glucose metabolism. Brain 124:1601–1609CrossRef
25.
go back to reference Greuel A, Pauls KAM, Koy A, Sudmeyer M, Schnitzler A, Timmermann L, Fink GR, Eggers C (2020) Pallidal deep brain stimulation reduces sensorimotor cortex activation in focal/segmental dystonia. Mov Disord 35(4):629–639CrossRef Greuel A, Pauls KAM, Koy A, Sudmeyer M, Schnitzler A, Timmermann L, Fink GR, Eggers C (2020) Pallidal deep brain stimulation reduces sensorimotor cortex activation in focal/segmental dystonia. Mov Disord 35(4):629–639CrossRef
26.
go back to reference Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 20:128–154CrossRef Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev 20:128–154CrossRef
27.
go back to reference Yelnik J (2002) Functional anatomy of the basal ganglia. Mov Disord 17(Suppl 3):S15–21CrossRef Yelnik J (2002) Functional anatomy of the basal ganglia. Mov Disord 17(Suppl 3):S15–21CrossRef
28.
go back to reference Haegelen C, Baumgarten C, Houvenaghel JF, Zhao Y, Peron J, Drapier S, Jannin P, Morandi X (2018) Functional atlases for analysis of motor and neuropsychological outcomes after medial globus pallidus and subthalamic stimulation. PLoS ONE 13:e0200262CrossRef Haegelen C, Baumgarten C, Houvenaghel JF, Zhao Y, Peron J, Drapier S, Jannin P, Morandi X (2018) Functional atlases for analysis of motor and neuropsychological outcomes after medial globus pallidus and subthalamic stimulation. PLoS ONE 13:e0200262CrossRef
Metadata
Title
Deep brain stimulation of the internal globus pallidus does not affect the limbic circuit in patients with Parkinson’s disease: a PET study
Authors
Xavier Palard-Novello
Sophie Drapier
Alexandre Bonnet
Antoine Girard
Gabriel Robert
Jean-François Houvenaghel
Paul Sauleau
Marc Vérin
Claire Haegelen
Florence Le Jeune
Publication date
01-02-2021
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 2/2021
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-020-10212-y

Other articles of this Issue 2/2021

Journal of Neurology 2/2021 Go to the issue