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Neuron. 2019 Mar 20;101(6):1109-1116.e5. doi: 10.1016/j.neuron.2019.01.019. Epub 2019 Feb 11.

Manipulation of Subcortical and Deep Cortical Activity in the Primate Brain Using Transcranial Focused Ultrasound Stimulation.

Author information

1
Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, UK; 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 OX3 9DU, UK. Electronic address: davide.folloni@psy.ox.ac.uk.
2
Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, UK; 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 OX3 9DU, UK. Electronic address: lennart.verhagen@psy.ox.ac.uk.
3
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 OX3 9DU, UK; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 HR Nijmegen, the Netherlands.
4
Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, UK; School of Psychology, University of Plymouth, Plymouth PL4 8AA, UK.
5
Physics for Medicine Paris, Inserm, ESPCI Paris, CNRS, PSL Research University, Univ Paris Diderot, Sorbonne Paris Cité, Paris 75012, France.
6
Physics for Medicine Paris, Inserm, ESPCI Paris, CNRS, PSL Research University, Paris 75012, France.
7
Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, UK; 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 OX3 9DU, UK.
8
Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford OX1 3SR, UK; 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 OX3 9DU, UK. Electronic address: jerome.sallet@psy.ox.ac.uk.

Abstract

The causal role of an area within a neural network can be determined by interfering with its activity and measuring the impact. Many current reversible manipulation techniques have limitations preventing their application, particularly in deep areas of the primate brain. Here, we demonstrate that a focused transcranial ultrasound stimulation (TUS) protocol impacts activity even in deep brain areas: a subcortical brain structure, the amygdala (experiment 1), and a deep cortical region, the anterior cingulate cortex (ACC, experiment 2), in macaques. TUS neuromodulatory effects were measured by examining relationships between activity in each area and the rest of the brain using functional magnetic resonance imaging (fMRI). In control conditions without sonication, activity in a given area is related to activity in interconnected regions, but such relationships are reduced after sonication, specifically for the targeted areas. Dissociable and focal effects on neural activity could not be explained by auditory confounds.

KEYWORDS:

amygdala; cingulate cortex; functional connectivity; limbic; macaque monkey; neuromodulation; resting-state connectivity; transcranial stimulation; ultrasound

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