Transcranial ultrasound stimulation effect in the redundant and synergistic networks consistent across macaques

Marilyn Gatica; Cyril Atkinson-Clement; Pedro A M Mediano; Mohammad Alkhawashki; James Ross; Jérôme Sallet; Marcus Kaiser

doi:10.1162/netn_a_00388

Transcranial ultrasound stimulation effect in the redundant and synergistic networks consistent across macaques

Netw Neurosci. 2024 Dec 10;8(4):1032-1050. doi: 10.1162/netn_a_00388. eCollection 2024.

Authors

Marilyn Gatica^{1

2}, Cyril Atkinson-Clement¹, Pedro A M Mediano^{3

4}, Mohammad Alkhawashki¹, James Ross¹, Jérôme Sallet^{5

6}, Marcus Kaiser^{1

7

8}

Affiliations

¹ Precision Imaging, School of Medicine, University of Nottingham, Nottingham, United Kingdom.
² NPLab, Network Science Institute, Northeastern University London, London, United Kingdom.
³ Department of Computing, Imperial College London, London, United Kingdom.
⁴ Division of Psychology and Language Sciences, University College London, London, United Kingdom.
⁵ Wellcome Centre for Integrative Neuroimaging (WIN), Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.
⁶ Univ Lyon, Université Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, Bron, France.
⁷ School of Computing Science, Newcastle University, Newcastle, United Kingdom.
⁸ Rui Jin Hospital, Shanghai Jiao Tong University, Shanghai, China.

Abstract

Low-intensity transcranial ultrasound stimulation (TUS) is a noninvasive technique that safely alters neural activity, reaching deep brain areas with good spatial accuracy. We investigated the effects of TUS in macaques using a recent metric, the synergy minus redundancy rank gradient, which quantifies different kinds of neural information processing. We analyzed this high-order quantity on the fMRI data after TUS in two targets: the supplementary motor area (SMA-TUS) and the frontal polar cortex (FPC-TUS). The TUS produced specific changes at the limbic network at FPC-TUS and the motor network at SMA-TUS and altered the sensorimotor, temporal, and frontal networks in both targets, mostly consistent across macaques. Moreover, there was a reduction in the structural and functional coupling after both stimulations. Finally, the TUS changed the intrinsic high-order network topology, decreasing the modular organization of the redundancy at SMA-TUS and increasing the synergistic integration at FPC-TUS.

Keywords: High-order; Redundancy; Synergy; TUS; fMRI.

Plain language summary

This article aims to elucidate how the transcranial ultrasound stimulation (TUS) could reorganize the brain as measured by the computation of redundancy and synergy. Our results showed that the TUS produced target-specific changes in the synergy minus redundancy rank gradient distribution at the limbic network at the frontal polar cortex (FPC-TUS) and the motor network at the supplementary motor area (SMA-TUS) and alterations in common, independent of the target, on the sensorimotor, temporal, and frontal networks. Moreover, the TUS changed the intrinsic high-order network topology, reducing the modular organization of the redundancy at SMA-TUS and increasing the synergistic integration at FPC-TUS.