Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus

Background: Brief transcranial focused ultrasound stimulation (tFUS) is used in cognitive mapping, where it is assumed that the intervention itself does not cause lasting modifications to the underlying networks being targeted. However, how so-called ‘offline’ effects impact the dynamic function of...

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Main Authors: William W. Watts, Benjamin Clennell, James K. Jiang, Konoha Izaki-Lee, Abhishek Binodh, Robyn Cuthell, Deniz Tonyali, Jon Crompton, Rosie Taaffe, Alanoud Alqahtani, Anna Andrieu, Igino Rafael Besinga, Kate Heesom, Tom G.J. Steward, Kwangwook Cho, Bruce W. Drinkwater, Elek Molnár, Daniel J. Whitcomb
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Brain Stimulation
Online Access:http://www.sciencedirect.com/science/article/pii/S1935861X25003079
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author William W. Watts
Benjamin Clennell
James K. Jiang
Konoha Izaki-Lee
Abhishek Binodh
Robyn Cuthell
Deniz Tonyali
Jon Crompton
Rosie Taaffe
Alanoud Alqahtani
Anna Andrieu
Igino Rafael Besinga
Kate Heesom
Tom G.J. Steward
Kwangwook Cho
Bruce W. Drinkwater
Elek Molnár
Daniel J. Whitcomb
author_facet William W. Watts
Benjamin Clennell
James K. Jiang
Konoha Izaki-Lee
Abhishek Binodh
Robyn Cuthell
Deniz Tonyali
Jon Crompton
Rosie Taaffe
Alanoud Alqahtani
Anna Andrieu
Igino Rafael Besinga
Kate Heesom
Tom G.J. Steward
Kwangwook Cho
Bruce W. Drinkwater
Elek Molnár
Daniel J. Whitcomb
author_sort William W. Watts
collection DOAJ
description Background: Brief transcranial focused ultrasound stimulation (tFUS) is used in cognitive mapping, where it is assumed that the intervention itself does not cause lasting modifications to the underlying networks being targeted. However, how so-called ‘offline’ effects impact the dynamic function of neural circuits is largely unknown. Objectives: To determine the persistent effects of ultrasound stimulation on hippocampal circuit function. Methods: Acute rat hippocampal slices in vitro, and rat hippocampi in vivo, were exposed to 40 s, 5 Hz pulsed ultrasound or sham stimulation. The effects of ultrasound on the dynamic synaptic and circuit function of the hippocampus were assessed through quantitative proteomics and extracellular field electrophysiology. Results: We find that ultrasound stimulation induces persistent and differential changes in protein expression and kinase activity in the hippocampus. This occurs concurrently with an enhancement of basal synaptic transmission and modifications to the susceptibility for the hippocampal circuit to undergo synaptic plasticity. These effects occur via a canonical Akt-dependent metaplastic process. Conclusion: The results indicate that tFUS can fundamentally modulate key signalling mechanisms that are responsible for determining the synaptic efficacy in a neural circuit. Importantly, these effects last beyond the duration of the stimulus. These findings provide a mechanistic insight into the sustained impact of tFUS on network function, and emphasise the importance of considering such effects in animal and human studies.
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spelling doaj-art-9fa3a816b9534a3a988b67f299c329492025-08-26T04:14:13ZengElsevierBrain Stimulation1935-861X2025-09-011851587159910.1016/j.brs.2025.08.014Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampusWilliam W. Watts0Benjamin Clennell1James K. Jiang2Konoha Izaki-Lee3Abhishek Binodh4Robyn Cuthell5Deniz Tonyali6Jon Crompton7Rosie Taaffe8Alanoud Alqahtani9Anna Andrieu10Igino Rafael Besinga11Kate Heesom12Tom G.J. Steward13Kwangwook Cho14Bruce W. Drinkwater15Elek Molnár16Daniel J. Whitcomb17Bristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UKDepartment of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, UK-Dementia Research Institute, Maurice Wohl Clinical Neuroscience Institute, King's College London, London, SE5 9NU, UKFaculty of Engineering, University of Bristol, Bristol, BS8 1TR, UKSchool of Physiology, Pharmacology and Neuroscience, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS8 1TD, UKBristol Medical School, Faculty of Health and Life Sciences, University of Bristol, Bristol, BS1 3NY, UK; Corresponding author.Background: Brief transcranial focused ultrasound stimulation (tFUS) is used in cognitive mapping, where it is assumed that the intervention itself does not cause lasting modifications to the underlying networks being targeted. However, how so-called ‘offline’ effects impact the dynamic function of neural circuits is largely unknown. Objectives: To determine the persistent effects of ultrasound stimulation on hippocampal circuit function. Methods: Acute rat hippocampal slices in vitro, and rat hippocampi in vivo, were exposed to 40 s, 5 Hz pulsed ultrasound or sham stimulation. The effects of ultrasound on the dynamic synaptic and circuit function of the hippocampus were assessed through quantitative proteomics and extracellular field electrophysiology. Results: We find that ultrasound stimulation induces persistent and differential changes in protein expression and kinase activity in the hippocampus. This occurs concurrently with an enhancement of basal synaptic transmission and modifications to the susceptibility for the hippocampal circuit to undergo synaptic plasticity. These effects occur via a canonical Akt-dependent metaplastic process. Conclusion: The results indicate that tFUS can fundamentally modulate key signalling mechanisms that are responsible for determining the synaptic efficacy in a neural circuit. Importantly, these effects last beyond the duration of the stimulus. These findings provide a mechanistic insight into the sustained impact of tFUS on network function, and emphasise the importance of considering such effects in animal and human studies.http://www.sciencedirect.com/science/article/pii/S1935861X25003079
spellingShingle William W. Watts
Benjamin Clennell
James K. Jiang
Konoha Izaki-Lee
Abhishek Binodh
Robyn Cuthell
Deniz Tonyali
Jon Crompton
Rosie Taaffe
Alanoud Alqahtani
Anna Andrieu
Igino Rafael Besinga
Kate Heesom
Tom G.J. Steward
Kwangwook Cho
Bruce W. Drinkwater
Elek Molnár
Daniel J. Whitcomb
Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
Brain Stimulation
title Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
title_full Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
title_fullStr Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
title_full_unstemmed Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
title_short Brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
title_sort brief transcranial focused ultrasound stimulation causes lasting modifications to the synaptic circuitry of the hippocampus
url http://www.sciencedirect.com/science/article/pii/S1935861X25003079
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