Modulation of limbic resting-state networks by subthalamic nucleus deep brain stimulation

Author:

Eraifej John1,Cabral Joana234,Fernandes Henrique M.4,Kahan Joshua5,He Shenghong6,Mancini Laura78,Thornton John78,White Mark78,Yousry Tarek78,Zrinzo Ludvic5,Akram Harith5,Limousin Patricia5,Foltynie Tom5,Aziz Tipu Z.1,Deco Gustavo91011,Kringelbach Morten3412,Green Alexander L.1

Affiliation:

1. Oxford Functional Neurosurgery Group, Nuffield Department of Surgical Sciences, University of Oxford, Oxford, United Kingdom

2. Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Braga, Portugal

3. Centre for Eudaimonia and Human Flourishing, Linacre College, University of Oxford, Oxford, United Kingdom

4. Center for Music in the Brain, Department of Clinical Medicine, Aarhus University, Aarhus, Denmark

5. Sobell Department for Motor Neurosciences and Movement Disorders, UCL Institute of Neurology, London, United Kingdom

6. MRC Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

7. Neuroradiological Academic Unit, Department of Brain Repair and Rehabilitation, UCL Institute of Neurology, University College London, London, United Kingdom

8. Lysholm Department of Neuroradiology, National Hospital for Neurology and Neurosurgery, UCLH NHS Foundation Trust, London, United Kingdom

9. Center for Brain and Cognition, Computational Neuroscience Group, Universitat Pompeu Fabra, Barcelona, Spain

10. Institució Catalana de la Recerca i Estudis Avançats, Barcelona, Spain

11. Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany

12. Department of Psychiatry, University of Oxford, Oxford, United Kingdom

Abstract

Abstract Beyond the established effects of subthalamic nucleus deep brain stimulation (STN-DBS) in reducing motor symptoms in Parkinson’s disease, recent evidence has highlighted the effect on non-motor symptoms. However, the impact of STN-DBS on disseminated networks remains unclear. This study aimed to perform a quantitative evaluation of network-specific modulation induced by STN-DBS using Leading Eigenvector Dynamics Analysis (LEiDA). We calculated the occupancy of resting-state networks (RSNs) in functional MRI data from 10 patients with Parkinson’s disease implanted with STN-DBS and statistically compared between ON and OFF conditions. STN-DBS was found to specifically modulate the occupancy of networks overlapping with limbic RSNs. STN-DBS significantly increased the occupancy of an orbitofrontal limbic subsystem with respect to both DBS OFF (p = 0.0057) and 49 age-matched healthy controls (p = 0.0033). Occupancy of a diffuse limbic RSN was increased with STN-DBS OFF when compared with healthy controls (p = 0.021), but not when STN-DBS was ON, which indicates rebalancing of this network. These results highlight the modulatory effect of STN-DBS on components of the limbic system, particularly within the orbitofrontal cortex, a structure associated with reward processing. These results reinforce the value of quantitative biomarkers of RSN activity in evaluating the disseminated impact of brain stimulation techniques and the personalization of therapeutic strategies.

Publisher

MIT Press

Subject

Applied Mathematics,Artificial Intelligence,Computer Science Applications,General Neuroscience

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