Prefrontal network engagement by deep brain stimulation in limbic hubs.

deep brain stimulation (DBS) gamma oscillations major depressive disorder (MDD) prefrontal networks stereo-EEG/intracranial recordings subcallosal cingulate ventral capsule/ventral striatum

Journal

Frontiers in human neuroscience
ISSN: 1662-5161
Titre abrégé: Front Hum Neurosci
Pays: Switzerland
ID NLM: 101477954

Informations de publication

Date de publication:
2023
Historique:
received: 08 09 2023
accepted: 26 12 2023
medline: 29 1 2024
pubmed: 29 1 2024
entrez: 29 1 2024
Statut: epublish

Résumé

Prefrontal circuits in the human brain play an important role in cognitive and affective processing. Neuromodulation therapies delivered to certain key hubs within these circuits are being used with increasing frequency to treat a host of neuropsychiatric disorders. However, the detailed neurophysiological effects of stimulation to these hubs are largely unknown. Here, we performed intracranial recordings across prefrontal networks while delivering electrical stimulation to two well-established white matter hubs involved in cognitive regulation and depression: the subcallosal cingulate (SCC) and ventral capsule/ventral striatum (VC/VS). We demonstrate a shared frontotemporal circuit consisting of the ventromedial prefrontal cortex, amygdala, and lateral orbitofrontal cortex where gamma oscillations are differentially modulated by stimulation target. Additionally, we found participant-specific responses to stimulation in the dorsal anterior cingulate cortex and demonstrate the capacity for further tuning of neural activity using current-steered stimulation. Our findings indicate a potential neurophysiological mechanism for the dissociable therapeutic effects seen across the SCC and VC/VS targets for psychiatric neuromodulation and our results lay the groundwork for personalized, network-guided neurostimulation therapy.

Identifiants

pubmed: 38283094
doi: 10.3389/fnhum.2023.1291315
pmc: PMC10813208
doi:

Types de publication

Journal Article

Langues

eng

Pagination

1291315

Informations de copyright

Copyright © 2024 Allawala, Bijanki, Oswalt, Mathura, Adkinson, Pirtle, Shofty, Robinson, Harrison, Mathew, Goodman, Pouratian, Sheth and Borton.

Déclaration de conflit d'intérêts

SS has consulting agreements with Boston Scientific, Neuropace, Abbott, and Zimmer Biomet, Varian Medical and Sensoria Therapeutics and is a co-founder for Motif Neurotech. NP was a consultant for Second Sight Medical Products, Abbott Laboratories, Boston Scientific, and Sensoria Therapeutics. WG has received donated devices from Medtronic, has consulted for Biohaven Pharmaceuticals and receives royalties from Nview, LLC. SM was supported through the use of resources and facilities at the Michael E. Debakey VA Medical Center, Houston, Texas and receives support from The Menninger Clinic. SM has served as a consultant to Allergan, Alkermes, Axsome Therapeutics, BioXcel Therapeutics, Clexio Biosciences, COMPASS Pathways, Eleusis, Engrail Therapeutics, Greenwich Biosciences, Intra-Cellular Therapies, Janssen, Levo Therapeutics, Perception Neurosciences, Praxis Precision Medicines, Neumora, Neurocrine, Relmada Therapeutics, Sage Therapeutics, Seelos Therapeutics, and Sunovion. He has received research support from Biohaven Pharmaceuticals, Boehringer-Ingelheim, Janssen, Merck, Sage Therapeutics, and VistaGen Therapeutics. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Auteurs

Anusha Allawala (A)

School of Engineering, Brown University, Providence, RI, United States.
Department of Neurological Surgery, University of California, San Francisco, San Francisco, CA, United States.

Kelly R Bijanki (KR)

Department of Neurosurgery, Baylor College of Medicine, Houston, TX, United States.

Denise Oswalt (D)

Department of Neurosurgery, University of Pennsylvania, Philadelphia, PA, United States.

Raissa K Mathura (RK)

Department of Neurosurgery, Baylor College of Medicine, Houston, TX, United States.

Joshua Adkinson (J)

Department of Neurosurgery, Baylor College of Medicine, Houston, TX, United States.

Victoria Pirtle (V)

Department of Neurosurgery, Baylor College of Medicine, Houston, TX, United States.

Ben Shofty (B)

Department of Neurosurgery, University of Utah, Salt Lake City, UT, United States.

Meghan Robinson (M)

Department of Neurosurgery, Baylor College of Medicine, Houston, TX, United States.

Matthew T Harrison (MT)

Division of Applied Mathematics, Brown University, Providence, RI, United States.

Sanjay J Mathew (SJ)

Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, United States.

Wayne K Goodman (WK)

Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, TX, United States.

Nader Pouratian (N)

Department of Neurological Surgery, UT Southwestern Medical Center, Dallas, TX, United States.

Sameer A Sheth (SA)

Department of Neurosurgery, Baylor College of Medicine, Houston, TX, United States.

David A Borton (DA)

School of Engineering, Brown University, Providence, RI, United States.
Department of Veterans Affairs, Center for Neurorestoration and Neurotechnology, Providence, RI, United States.

Classifications MeSH