State-dependent Neurovascular Modulation Induced by Transcranial Ultrasound Stimulation

Overview

Journal Med Biol Eng Comput

Publisher Springer

Date 2025 Jan 27

PMID 39870987

Authors

Hang Song

Ruoyu Chen

Liyuan Ren

Junfeng Sun

Shanbao Tong

Affiliations

Soon will be listed here.

Abstract

Previous studies reported baseline state-dependent effects on neural and hemodynamic responses to transcranial ultrasound stimulation. However, due to neurovascular coupling, neither neural nor hemodynamic baseline alone can fully explain the ultrasound-induced responses. In this study, using a general linear model, we aimed to investigate the roles of both neural and hemodynamic baseline status as well as their interactions in ultrasound-induced responses. Thirty Sprague-Dawley rats were randomly assigned to Hypoxia, Hyperoxia, and Normoxia groups. The baseline states were altered by changing the oxygen concentrations. Micro-electrode and laser speckle contrast imaging were used to record local field potentials and cerebral blood flow during resting, before, and after ultrasound stimulation, respectively. We found that baseline neural activity played a positive role in neural response (Coefficient = 0.634, t = 1.748, p = 0.096, = 0.133), but a negative role in hemodynamic response (Coefficient = 0.060, t = 1.996, p = 0.060, = 0.166). Baseline hemodynamic activity also had a significantly negative correlation with the hemodynamic response (Coefficient = 0.760, t = 3.947, p 0.001, = 0.438). This study enriched our understanding of state-dependent effects underlying the neurovascular activation by ultrasound stimulation.

References

Blackmore J, Shrivastava S, Sallet J, Butler C, Cleveland R . Ultrasound Neuromodulation: A Review of Results, Mechanisms and Safety. Ultrasound Med Biol. 2019; 45(7):1509-1536. PMC: 6996285. DOI: 10.1016/j.ultrasmedbio.2018.12.015. View

Javid A, Ilham S, Kiani M . A Review of Ultrasound Neuromodulation Technologies. IEEE Trans Biomed Circuits Syst. 2023; 17(5):1084-1096. DOI: 10.1109/TBCAS.2023.3299750. View

Naor O, Krupa S, Shoham S . Ultrasonic neuromodulation. J Neural Eng. 2016; 13(3):031003. DOI: 10.1088/1741-2560/13/3/031003. View

Fomenko A, Neudorfer C, Dallapiazza R, Kalia S, Lozano A . Low-intensity ultrasound neuromodulation: An overview of mechanisms and emerging human applications. Brain Stimul. 2018; 11(6):1209-1217. DOI: 10.1016/j.brs.2018.08.013. View

Yuan Y, Zhao Y, Jia H, Liu M, Hu S, Li Y . Cortical Hemodynamic Responses Under Focused Ultrasound Stimulation Using Real-Time Laser Speckle Contrast Imaging. Front Neurosci. 2018; 12:269. PMC: 5925215. DOI: 10.3389/fnins.2018.00269. View

Wang X, Yan J, Wang Z, Li X, Yuan Y . Neuromodulation Effects of Ultrasound Stimulation Under Different Parameters on Mouse Motor Cortex. IEEE Trans Biomed Eng. 2019; 67(1):291-297. DOI: 10.1109/TBME.2019.2912840. View

Yu K, Niu X, Krook-Magnuson E, He B . Intrinsic functional neuron-type selectivity of transcranial focused ultrasound neuromodulation. Nat Commun. 2021; 12(1):2519. PMC: 8097024. DOI: 10.1038/s41467-021-22743-7. View

Sarica C, Nankoo J, Fomenko A, Grippe T, Yamamoto K, Samuel N . Human Studies of Transcranial Ultrasound neuromodulation: A systematic review of effectiveness and safety. Brain Stimul. 2022; 15(3):737-746. DOI: 10.1016/j.brs.2022.05.002. View

Zeng K, Li Z, Xia X, Wang Z, Darmani G, Li X . Effects of different sonication parameters of theta burst transcranial ultrasound stimulation on human motor cortex. Brain Stimul. 2024; 17(2):258-268. DOI: 10.1016/j.brs.2024.03.001. View

10.

Yuan Y, Zhang K, Zhang Y, Yan J, Wang Z, Wang X . The Effect of Low-Intensity Transcranial Ultrasound Stimulation on Neural Oscillation and Hemodynamics in the Mouse Visual Cortex Depends on Anesthesia Level and Ultrasound Intensity. IEEE Trans Biomed Eng. 2021; 68(5):1619-1626. DOI: 10.1109/TBME.2021.3050797. View

11.

Yang P, Phipps M, Jonathan S, Newton A, Byun N, Gore J . Bidirectional and state-dependent modulation of brain activity by transcranial focused ultrasound in non-human primates. Brain Stimul. 2021; 14(2):261-272. PMC: 7988301. DOI: 10.1016/j.brs.2021.01.006. View

12.

Wang X, Zhang Y, Zhang K, Yuan Y . Influence of behavioral state on the neuromodulatory effect of low-intensity transcranial ultrasound stimulation on hippocampal CA1 in mouse. Neuroimage. 2021; 241:118441. DOI: 10.1016/j.neuroimage.2021.118441. View

13.

DellItalia J, Sanguinetti J, Monti M, Bystritsky A, Reggente N . Current State of Potential Mechanisms Supporting Low Intensity Focused Ultrasound for Neuromodulation. Front Hum Neurosci. 2022; 16:872639. PMC: 9081930. DOI: 10.3389/fnhum.2022.872639. View

14.

McCormick D, Nestvogel D, He B . Neuromodulation of Brain State and Behavior. Annu Rev Neurosci. 2020; 43:391-415. DOI: 10.1146/annurev-neuro-100219-105424. View

15.

Silvanto J, Muggleton N, Walsh V . State-dependency in brain stimulation studies of perception and cognition. Trends Cogn Sci. 2008; 12(12):447-54. DOI: 10.1016/j.tics.2008.09.004. View

16.

Lee S, Dan Y . Neuromodulation of brain states. Neuron. 2012; 76(1):209-22. PMC: 3579548. DOI: 10.1016/j.neuron.2012.09.012. View

17.

Bradley C, Nydam A, Dux P, Mattingley J . State-dependent effects of neural stimulation on brain function and cognition. Nat Rev Neurosci. 2022; 23(8):459-475. DOI: 10.1038/s41583-022-00598-1. View

18.

Yang P, Phipps M, Newton A, Jonathan S, Manuel T, Gore J . Differential dose responses of transcranial focused ultrasound at brain regions indicate causal interactions. Brain Stimul. 2022; 15(6):1552-1564. PMC: 9806861. DOI: 10.1016/j.brs.2022.12.003. View

19.

Yuan Y, Wang Z, Wang X, Yan J, Liu M, Li X . Low-Intensity Pulsed Ultrasound Stimulation Induces Coupling Between Ripple Neural Activity and Hemodynamics in the Mouse Visual Cortex. Cereb Cortex. 2018; 29(7):3220-3223. DOI: 10.1093/cercor/bhy187. View

20.

Su Z, Liu M, Yuan Y, Jiao H . Transcranial ultrasound stimulation selectively affects cortical neurovascular coupling across neuronal types and LFP frequency bands. Cereb Cortex. 2023; 34(1). DOI: 10.1093/cercor/bhad465. View