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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

Network Neuroscience 2024 · 10.1162/netn_a_00388

nonhuman primatehealthyfmri

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.

Abstract via europepmc.

Speciesmacaque
Subjects3 animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlinactive transducer
Auditory controlnot reported
Readout timingoffline
Anaesthesiaanaesthetised
Readoutsfmri — redundancy/synergy (synergy minus redundancy rank gradient) analysis of resting fMRI
Direction of effectmixed or unclearTUS shifted regions toward either redundancy or synergy depending on region and target; the effect is not classed as excitatory or inhibitory.
Adverse eventsnot reported

Exposures

Exposure 1: SMA-TUS

Target: supplementary motor area — “supplementary motor area (SMA)”
Device: Sonic Concepts · Sonic Concepts · H115-MR ✓

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓✓
Pulse duration (ms)30✓✓✓⚑
Pulse repetition frequency (Hz)10✓✓✓
Duty cycle (%)not reportedpulse duration × PRF gives 30%
Sonication duration (s)40✓✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)1,170, 1,350swept✓✓✓⚑
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatenot reported
In-situ pressure (kPa)880✓✓✓
In-situ Isppa (W/cm²)24.1✓✓✓
In-situ Ispta (W/cm²)7.2✓✓✓
Protocol, in the paper’s words

30-ms bursts of ultrasound every 100 ms for 40 s, both hemispheres at once with a single train, offline TUS then fMRI; at least 10 days between TUS sessions.

Exposure 2: FPC-TUS

Target: anterior prefrontal cortex — “frontal polar cortex (FPC)”
Device: Sonic Concepts · Sonic Concepts · H115-MR ✓

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓✓
Pulse duration (ms)30✓✓✓
Pulse repetition frequency (Hz)10✓✓✓
Duty cycle (%)not reportedpulse duration × PRF gives 30%
Sonication duration (s)40✓✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)1,170, 1,350swept✓✓✓
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)31.7✓✓✓
In-situ Ispta (W/cm²)9.5✓✓✓
Protocol, in the paper’s words

30-ms bursts of ultrasound every 100 ms for 40 s, both hemispheres at once with a single train, offline TUS then fMRI; at least 10 days between TUS sessions.

Flags from extraction

  • exposures[0].free_field.pressure_kpa — Pressure range 1.17-1.35 MPa is given for voltage range across sessions and is not assigned to a target; it applies to both exposures. Disagrees with 0.88 MPa Pmax stated for SMA.
  • exposures[0].unspecified_domain.pressure_kpa — 0.88 MPa 'maximum peak pressure at the acoustic focus point estimation'; domain not stated.
  • exposures[1].unspecified_domain.isppa_w_cm2 — FPC intensities given without a domain; no FPC pressure stated separately.
  • exposures[0].timing.pulse_duration_ms — 30-ms bursts every 100 ms; burst taken as the pulse. Duty cycle not stated.
  • n_subjects — Secondary analysis of an earlier macaque dataset (Verhagen et al. 2019); stimulation details are quoted from the present methods.
  • n_sessions_per_subject — Three MRI sessions per condition per macaque are described; TUS session count not stated plainly.