A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation
Background: Obsessive-compulsive disorder (OCD) has consistently been linked to abnormal frontostriatal activity. The electrophysiological disruption in this circuit, however, remains to be characterized. Objective/hypothesis: The primary goal of this study was to investigate the neuronal synchroniz...
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| Format: | Article |
| Language: | English |
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Elsevier
2021-07-01
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| Series: | Brain Stimulation |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X21000991 |
| _version_ | 1818917844133347328 |
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| author | Svenja Treu Javier J. Gonzalez-Rosa Vanesa Soto-Leon Diego Lozano-Soldevilla Antonio Oliviero Fernando Lopez-Sosa Blanca Reneses-Prieto Juan A. Barcia Bryan A. Strange |
| author_facet | Svenja Treu Javier J. Gonzalez-Rosa Vanesa Soto-Leon Diego Lozano-Soldevilla Antonio Oliviero Fernando Lopez-Sosa Blanca Reneses-Prieto Juan A. Barcia Bryan A. Strange |
| author_sort | Svenja Treu |
| collection | DOAJ |
| description | Background: Obsessive-compulsive disorder (OCD) has consistently been linked to abnormal frontostriatal activity. The electrophysiological disruption in this circuit, however, remains to be characterized. Objective/hypothesis: The primary goal of this study was to investigate the neuronal synchronization in OCD patients. We predicted aberrant oscillatory activity in frontal regions compared to healthy control subjects, which would be alleviated by deep brain stimulation (DBS) of the nucleus accumbens (NAc). Methods: We compared scalp EEG recordings from nine patients with OCD treated with NAc-DBS with recordings from healthy controls, matched for age and gender. Within the patient group, EEG activity was compared with DBS turned off vs. stimulation at typical clinical settings (3.5 V, frequency of stimulation 130 Hz, pulse width 60 μs). In addition, intracranial EEG was recorded directly from depth macroelectrodes in the NAc in four OCD patients. Results: Cross-frequency coupling between the phase of alpha/low beta oscillations and amplitude of high gamma was significantly increased over midline frontal and parietal electrodes in patients when stimulation was turned off, compared to controls. Critically, in patients, beta (16–25 Hz) -gamma (110–166 Hz) phase amplitude coupling source localized to the ventromedial prefrontal cortex, and was reduced when NAc-DBS was active. In contrast, intracranial EEG recordings showed no beta-gamma phase amplitude coupling. The contribution of non-sinusoidal beta waveforms to this coupling are reported. Conclusion: We reveal an increased beta-gamma phase amplitude coupling in fronto-central scalp sensors in patients suffering from OCD, compared to healthy controls, which may derive from ventromedial prefrontal regions implicated in OCD and is normalized by DBS of the nucleus accumbens. This aberrant cross-frequency coupling could represent a biomarker of OCD, as well as a target for novel therapeutic approaches. |
| first_indexed | 2024-12-20T00:40:31Z |
| format | Article |
| id | doaj.art-2a8930c2fe754559bc4d99e32ac85bab |
| institution | Directory Open Access Journal |
| issn | 1935-861X |
| language | English |
| last_indexed | 2024-12-20T00:40:31Z |
| publishDate | 2021-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj.art-2a8930c2fe754559bc4d99e32ac85bab2022-12-21T19:59:37ZengElsevierBrain Stimulation1935-861X2021-07-01144761770A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulationSvenja Treu0Javier J. Gonzalez-Rosa1Vanesa Soto-Leon2Diego Lozano-Soldevilla3Antonio Oliviero4Fernando Lopez-Sosa5Blanca Reneses-Prieto6Juan A. Barcia7Bryan A. Strange8Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Spain; Corresponding author. Laboratory for Clinical Neuroscience, Universidad Politécnica de Madrid, Centro de Tecnología Biomédica, Parque Científico y Tecnológico de la U.P.M. Campus de Montegancedo. Ctra. M 40-Km.38, 28223 Pozuelo de Alarcón. Madrid, Spain.;Laboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Spain; University of Cadiz, Institute of Biomedical Research Cadiz (INiBICA), Cádiz, SpainHospital Nacional de Parapléjicos, FENNSI Group, Hospital Nacional de Parapléjicos, Toledo, SpainLaboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, SpainHospital Nacional de Parapléjicos, FENNSI Group, Hospital Nacional de Parapléjicos, Toledo, SpainLaboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, Spain; University of Cadiz, Institute of Biomedical Research Cadiz (INiBICA), Cádiz, SpainDepartment of Psychiatry, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos, Universidad Complutense de Madrid, SpainDepartment of Neurosurgery, Hospital Clínico San Carlos, Instituto de Investigación Sanitaria San Carlos, Universidad Complutense de Madrid, SpainLaboratory for Clinical Neuroscience, Centre for Biomedical Technology, Universidad Politécnica de Madrid, SpainBackground: Obsessive-compulsive disorder (OCD) has consistently been linked to abnormal frontostriatal activity. The electrophysiological disruption in this circuit, however, remains to be characterized. Objective/hypothesis: The primary goal of this study was to investigate the neuronal synchronization in OCD patients. We predicted aberrant oscillatory activity in frontal regions compared to healthy control subjects, which would be alleviated by deep brain stimulation (DBS) of the nucleus accumbens (NAc). Methods: We compared scalp EEG recordings from nine patients with OCD treated with NAc-DBS with recordings from healthy controls, matched for age and gender. Within the patient group, EEG activity was compared with DBS turned off vs. stimulation at typical clinical settings (3.5 V, frequency of stimulation 130 Hz, pulse width 60 μs). In addition, intracranial EEG was recorded directly from depth macroelectrodes in the NAc in four OCD patients. Results: Cross-frequency coupling between the phase of alpha/low beta oscillations and amplitude of high gamma was significantly increased over midline frontal and parietal electrodes in patients when stimulation was turned off, compared to controls. Critically, in patients, beta (16–25 Hz) -gamma (110–166 Hz) phase amplitude coupling source localized to the ventromedial prefrontal cortex, and was reduced when NAc-DBS was active. In contrast, intracranial EEG recordings showed no beta-gamma phase amplitude coupling. The contribution of non-sinusoidal beta waveforms to this coupling are reported. Conclusion: We reveal an increased beta-gamma phase amplitude coupling in fronto-central scalp sensors in patients suffering from OCD, compared to healthy controls, which may derive from ventromedial prefrontal regions implicated in OCD and is normalized by DBS of the nucleus accumbens. This aberrant cross-frequency coupling could represent a biomarker of OCD, as well as a target for novel therapeutic approaches.http://www.sciencedirect.com/science/article/pii/S1935861X21000991Obsessive-compulsive disorderDeep brain stimulationEEGNucleus accumbensVentromedial frontal cross-frequency coupling |
| spellingShingle | Svenja Treu Javier J. Gonzalez-Rosa Vanesa Soto-Leon Diego Lozano-Soldevilla Antonio Oliviero Fernando Lopez-Sosa Blanca Reneses-Prieto Juan A. Barcia Bryan A. Strange A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation Brain Stimulation Obsessive-compulsive disorder Deep brain stimulation EEG Nucleus accumbens Ventromedial frontal cross-frequency coupling |
| title | A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation |
| title_full | A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation |
| title_fullStr | A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation |
| title_full_unstemmed | A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation |
| title_short | A ventromedial prefrontal dysrhythmia in obsessive-compulsive disorder is attenuated by nucleus accumbens deep brain stimulation |
| title_sort | ventromedial prefrontal dysrhythmia in obsessive compulsive disorder is attenuated by nucleus accumbens deep brain stimulation |
| topic | Obsessive-compulsive disorder Deep brain stimulation EEG Nucleus accumbens Ventromedial frontal cross-frequency coupling |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X21000991 |
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