Offline impact of transcranial focused ultrasound on cortical activation in primates

Author:

Verhagen Lennart12ORCID,Gallea Cécile3,Folloni Davide12ORCID,Constans Charlotte4ORCID,Jensen Daria EA12,Ahnine Harry3,Roumazeilles Léa12,Santin Mathieu3,Ahmed Bashir5,Lehericy Stéphane3,Klein-Flügge Miriam C12ORCID,Krug Kristine5ORCID,Mars Rogier B26,Rushworth Matthew FS12,Pouget Pierre7ORCID,Aubry Jean-François8ORCID,Sallet Jerome12ORCID

Affiliation:

1. Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom

2. Wellcome Centre for Integrative Neuroimaging (WIN), Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford, United Kingdom

3. Institute du Cerveau et de la Moelle épinière (ICM), Centre for NeuroImaging Research (CENIR), Inserm U 1127, CNRS UMR 7225, Sorbonne Université, Paris, France

4. Physics for Medicine Paris, Inserm, ESPCI Paris, CNRS, PSL Research University, Université Paris Diderot, Sorbonne Paris Cité, Paris, France

5. Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom

6. Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands

7. Institute du Cerveau et de la Moelle épinière (ICM), UMRS 975 INSERM, CNRS 7225, UMPC, Paris, France

8. Physics for Medicine Paris, Inserm, ESPCI Paris, CNRS, PSL Research University, Paris, France

Abstract

To understand brain circuits it is necessary both to record and manipulate their activity. Transcranial ultrasound stimulation (TUS) is a promising non-invasive brain stimulation technique. To date, investigations report short-lived neuromodulatory effects, but to deliver on its full potential for research and therapy, ultrasound protocols are required that induce longer-lasting ‘offline’ changes. Here, we present a TUS protocol that modulates brain activation in macaques for more than one hour after 40 s of stimulation, while circumventing auditory confounds. Normally activity in brain areas reflects activity in interconnected regions but TUS caused stimulated areas to interact more selectively with the rest of the brain. In a within-subject design, we observe regionally specific TUS effects for two medial frontal brain regions – supplementary motor area and frontal polar cortex. Independently of these site-specific effects, TUS also induced signal changes in the meningeal compartment. TUS effects were temporary and not associated with microstructural changes.

Funder

Wellcome

Bettencourt Schueller Foundation

Agence Nationale de la Recherche

Medical Research Council

Biotechnology and Biological Sciences Research Council

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

Reference89 articles.

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3. Experimental demonstration of noninvasive transskull adaptive focusing based on prior computed tomography scans;Aubry;The Journal of the Acoustical Society of America,2003

4. Prefrontal connections of medial motor areas in the rhesus monkey;Bates;The Journal of Comparative Neurology,1993

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