Theta-alpha oscillations characterize emotional subregion in the human ventral subthalamic nucleus.
Parkinson's disease
deep brain stimulation
oscillations
subthalamic nucleus
Journal
Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
10
06
2019
revised:
22
09
2019
accepted:
27
09
2019
pubmed:
24
11
2019
medline:
16
1
2021
entrez:
24
11
2019
Statut:
ppublish
Résumé
Therapeutic outcomes of STN-DBS for movement and psychiatric disorders depend on electrode location within the STN. Electrophysiological and functional mapping of the STN has progressed considerably in the past years, identifying beta-band oscillatory activity in the dorsal STN as a motor biomarker. It also has been suggested that STN theta-alpha oscillations, involved in impulse control and action inhibition, have a ventral source. However, STN local field potential mapping of motor, associative, and limbic areas is often limited by poor spatial resolution. Providing a high-resolution electrophysiological map of the motor, associative and limbic anatomical sub-areas of the subthalamic nucleus. We have analyzed high-spatial-resolution STN microelectrode electrophysiology recordings of PD patients (n = 303) that underwent DBS surgery. The patients' STN intraoperative recordings of spiking activity (933 electrode trajectories) were combined with their imaging data (n = 83 patients, 151 trajectories). We found a high theta-alpha (7-10 Hz) oscillatory area, located near the STN ventromedial border in 29% of the PD patients. Theta-alpha activity in this area has higher power and lower central frequency in comparison to theta-alpha activity in more dorsal subthalamic areas. When projected on the DISTAL functional atlas, the theta-alpha oscillatory area overlaps with the STN limbic subarea. We suggest that theta-alpha oscillations can serve as an electrophysiological marker for the ventral subthalamic nucleus limbic subarea. Therefore, theta-alpha oscillations can guide optimal electrode placement in neuropsychiatric STN-DBS procedures and provide a reliable biomarker input for future closed-loop DBS device. © 2019 International Parkinson and Movement Disorder Society.
Sections du résumé
BACKGROUND
Therapeutic outcomes of STN-DBS for movement and psychiatric disorders depend on electrode location within the STN. Electrophysiological and functional mapping of the STN has progressed considerably in the past years, identifying beta-band oscillatory activity in the dorsal STN as a motor biomarker. It also has been suggested that STN theta-alpha oscillations, involved in impulse control and action inhibition, have a ventral source. However, STN local field potential mapping of motor, associative, and limbic areas is often limited by poor spatial resolution.
OBJECTIVES
Providing a high-resolution electrophysiological map of the motor, associative and limbic anatomical sub-areas of the subthalamic nucleus.
METHODS
We have analyzed high-spatial-resolution STN microelectrode electrophysiology recordings of PD patients (n = 303) that underwent DBS surgery. The patients' STN intraoperative recordings of spiking activity (933 electrode trajectories) were combined with their imaging data (n = 83 patients, 151 trajectories).
RESULTS
We found a high theta-alpha (7-10 Hz) oscillatory area, located near the STN ventromedial border in 29% of the PD patients. Theta-alpha activity in this area has higher power and lower central frequency in comparison to theta-alpha activity in more dorsal subthalamic areas. When projected on the DISTAL functional atlas, the theta-alpha oscillatory area overlaps with the STN limbic subarea.
CONCLUSIONS
We suggest that theta-alpha oscillations can serve as an electrophysiological marker for the ventral subthalamic nucleus limbic subarea. Therefore, theta-alpha oscillations can guide optimal electrode placement in neuropsychiatric STN-DBS procedures and provide a reliable biomarker input for future closed-loop DBS device. © 2019 International Parkinson and Movement Disorder Society.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
337-343Informations de copyright
© 2019 International Parkinson and Movement Disorder Society.
Références
Limousin P, Pollak P, Benazzouz A, Hoffmann D, Broussolle E, Perret JE, Benabid A-L. Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov Disord 1995;10:672-674.
Krack P, Batir A, Van Blercom N, et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 20013;349:1925-1934.
Parent A, Hazrati LN. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry. Brain Res Rev 1995;20:128-154.
Haynes WIA, Haber SN. The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for basal ganglia models and deep brain stimulation. J Neurosci 2013;33:4804-4814.
Lambert C, Zrinzo L, Nagy Z, et al. Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. Neuroimage 2012;60:83-94.
Ewert S, Plettig P, Li N, et al. Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. Neuroimage 2018;170:271-282.
Mallet L, Schüpbach M, N'Diaye K, et al. Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior. Proc Natl Acad Sci USA 2007;104:10661-10666.
Eitan R, Shamir RR, Linetsky E, et al. Asymmetric right/left encoding of emotions in the human subthalamic nucleus. Front Syst Neurosci 2013;7:69.
Hamani C, Florence G, Heinsen H, et al. Subthalamic nucleus deep brain stimulation: basic concepts and novel perspectives. Eneuro 2017;4:ENEURO.0140-17.2017.
Starr PA. Placement of deep brain stimulators into the subthalamic nucleus or globus pallidus internus: technical approach. Stereotact Funct Neurosurg 2002;79:118-145.
Wodarg F, Herzog J, Reese R, et al. Stimulation site within the MRI-defined STN predicts postoperative motor outcome. Mov Disord 2012;27:874-879.
Zaidel A, Spivak A, Grieb B, Bergman H, Israel Z. Subthalamic span of beta oscillations predicts deep brain stimulation efficacy for patients with Parkinson's disease. Brain 2010;133:2007-2021.
Castrioto A, Lhommée E, Moro E, Krack P. Mood and behavioural effects of subthalamic stimulation in Parkinson's disease. Lancet Neurol 2014;13:287-305.
Horn A, Neumann WJ, Degen K, Schneider GH, Kühn AA. Toward an electrophysiological “sweet spot” for deep brain stimulation in the subthalamic nucleus. Hum Brain Mapp 2017;38:3377-3390.
Accolla EA, Horn A, Herrojo-Ruiz M, Neumann WJ, Kühn AA. Reply: oscillatory coupling of the subthalamic nucleus in obsessive compulsive disorder. Brain 2017;140:e57.
Marmor O, Valsky D, Joshua M, et al. Local vs. volume conductance activity of field potentials in the human subthalamic nucleus. J Neurophysiol 2017;117:2140-2151.
Machado A, Rezai AR, Kopell BH, Gross RE, Sharan AD, Benabid A-L. Deep brain stimulation for Parkinson's disease: surgical technique and perioperative management. Mov Disord 2006;21(Suppl. 14):S247-S258.
Tamir I, Marmor-Levin O, Eitan R, Bergman H, Israel Z. Posterolateral trajectories favor a longer motor domain in subthalamic nucleus deep brain stimulation for Parkinson disease. World Neurosurg 2017;106:450-461.
Zaidel A, Spivak A, Shpigelman L, Bergman H, Israel Z. Delimiting subterritories of the human subthalamic nucleus by means of microelectrode recordings and a Hidden Markov Model. Mov Disord 2009;24:1785-1793.
Valsky D, Marmor-Levin O, Deffains M, Eitan R, Blackwell KT, Bergman H, Israel Z. Stop! border ahead: automatic detection of subthalamic exit during deep brain stimulation surgery. Mov Disord 2017;32:70-79.
Horn A, Li N, Dembek TA, et al. Lead-DBS v2: towards a comprehensive pipeline for deep brain stimulation imaging. Neuroimage 2019;184:293-316.
Maris E, Oostenveld R. Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 2007;164:177-190.
Geng X, Xu X, Horn A, Li N, Ling Z, Brown P, Wang S. Intra-operative characterisation of subthalamic oscillations in Parkinson's disease. Clin Neurophysiol 2018;129:1001-1010.
Zavala B, Zaghloul K, Brown P. The subthalamic nucleus, oscillations, and conflict. Mov Disord 2015;30:328-338.
Brittain JS, Watkins KE, Joundi RA, et al. A role for the subthalamic nucleus in response inhibition during conflict. J Neurosci 2012;32:13396-13401.
Zavala B, Brittain J-S, Jenkinson N, et al. Subthalamic nucleus local field potential activity during the Eriksen Flanker task reveals a novel role for theta phase during conflict monitoring. J Neurosci 2013;33:14758-14766.
Zavala BA, Tan H, Little S, et al. Midline frontal cortex low-frequency activity drives subthalamic nucleus oscillations during conflict. J Neurosci 2014;34:7322-7333.
Rosa M, Fumagalli M, Giannicola G, et al. Pathological gambling in Parkinson's disease: subthalamic oscillations during economics decisions. Mov Disord 2013;28:1644-1652.
Fumagalli M, Giannicola G, Rosa M, et al. Conflict-dependent dynamic of subthalamic nucleus oscillations during moral decisions. Soc Neurosci 2011;6:243-256.
Rodriguez-Oroz MC, López-Azcárate J, Garcia-Garcia D, et al. Involvement of the subthalamic nucleus in impulse control disorders associated with Parkinson's disease. Brain 2011;134:36-49.