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The effect of transcranial ultrasound pulse repetition frequency on sustained inhibition in the human primary motor cortex: A double-blind, sham-controlled study

Ali K. Zadeh, Hrishikesh Raghuram, Shirshak Shrestha, Mekale Kibreab, Iris Kathol, Davide Martino, G. Bruce Pike, Samuel Pichardo, Oury Monchi

Brain Stimulation 2024, 17, 476-484 · 10.1016/j.brs.2024.04.005

human healthyhealthyemg mep

Abstract

Background Non-invasive brain stimulation techniques such as transcranial magnetic stimulation and transcranial direct current stimulation hold promise for inducing brain plasticity. However, their limited precision may hamper certain applications. In contrast, Transcranial Ultrasound Stimulation (TUS), known for its precision and deep brain targeting capabilities, requires further investigation to establish its efficacy in producing enduring effects for treating neurological and psychiatric disorders. Objective To investigate the enduring effects of different pulse repetition frequencies (PRF) of TUS on motor corticospinal excitability. Methods T1-, T2-weighted, and zero echo time magnetic resonance imaging scans were acquired from 21 neurologically healthy participants for neuronavigation, skull reconstruction, and the performance of transcranial ultrasound and thermal modelling. The effects of three different TUS PRFs (10, 100, and 1000 Hz) with a constant duty cycle of 10 % on corticospinal excitability in the primary motor cortex were assessed using TMS-induced motor evoked potentials (MEPs). Each PRF and sham condition was evaluated on separate days, with measurements taken 5-, 30-, and 60-min post-TUS. Results A significant decrease in MEP amplitude was observed with a PRF of 10 Hz (p = 0.007), which persisted for at least 30 min, and with a PRF of 100 Hz (p = 0.001), lasting over 60 min. However, no significant changes were found for the PRF of 1000 Hz and the sham conditions. Conclusion This study highlights the significance of PRF selection in TUS and underscores its potential as a non-invasive approach to reduce corticospinal excitability, offering valuable insights for future clinical applications.

Abstract via europepmc.

Specieshuman
Subjects25 participants
Sessions per subject4
Randomisedyes
Blindingdouble
Sham / controlinactive transducer
Auditory controlramped pulses
Readout timingoffline
Anaesthesianot applicable
Readoutsemg mepTMS-induced motor-evoked potential (MEP) amplitude and latency; resting motor threshold (RMT)
Direction of effectinhibitoryPRFs of 10 Hz and 100 Hz produced significant, sustained decreases in MEP amplitude (inhibition), lasting at least 30 min and over 60 min respectively; 1000 Hz PRF and sham produced no significant change.
Adverse eventsobservedParticipants reported mild-to-moderate symptoms possibly/probably related to stimulation across active and sham conditions; none were rated severe or definitely related to TUS. Maximum predicted brain temperature increase was 0.3-0.99 C and predicted mechanical index ranged 0.44-1.19, both within FDA guidelines.

Exposures

Exposure 1: TUS of left primary motor cortex at 10/100/1000 Hz PRF

Target: primary motor cortex — “primary motor cortex
Device: Sonic Concepts · Sonic Concepts · H317 (128-element phased array)

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)not reported
Pulse repetition frequency (Hz)10, 100, 1,000swept✓✓
Duty cycle (%)10✓✓
Sonication duration (s)120✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)980✓✓
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatesimulationsingle value
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)5✓✓
In-situ Ispta (W/cm²)0.5✓✓
Protocol, in the paper’s words

Ultrasound delivery in all stimulation sessions consisted of a 120-s train with a DC of 10%, driven at a fundamental frequency of 250 kHz. A total ramping of 25% of the burst duration (12.5% up, 12.5% down) was applied to all PRF conditions to reduce auditory confounds. Each PRF (10, 100, 1000 Hz) and a sham condition were tested on separate days in randomised order; MEPs were assessed at baseline and 5, 30 and 60 min post-TUS.

Flags from extraction

  • n_subjects25 individuals enrolled but 4 withdrew during stimulation visits (irregular attendance, inability to relax, dizziness during TMS), leaving 21 who completed all sessions and were analysed; enrolled figure (25) recorded per enrolled-vs-analysed convention.
  • exposures[0].free_field.pressure_kpaThe 0.98 MPa value comes from the calibration procedure performed at PRF 100 Hz / DC 2% (50-cycle burst) used for focus characterization, not explicitly confirmed as the free-field pressure delivered during the actual DC 10% experimental protocol.
  • exposures[0].in_situ.isppa_w_cm2The corresponding sentence in the main Methods text has an OCR/typesetting artefact that drops the numeral; the value (5 W/cm2) is only clearly legible in the Fig. 2 caption text, which was used as the quote.
  • exposures[0].timing.pulse_duration_msPaper states duty cycle (10%) and PRF (10/100/1000 Hz) but never states pulse duration directly; left not_reported rather than computed from duty_cycle/PRF.