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Excitatory‐inhibitory modulation of transcranial focus ultrasound stimulation on human motor cortex

Tingting Zhang, Bingqi Guo, Zhentao Zuo, Xiaojing Long, Shimin Hu, Siran Li, Xin Su, Yuping Wang, Chunyan Liu

CNS Neuroscience & Therapeutics 2023, 29, 3829-3841 · 10.1111/cns.14303

human healthyhealthyemg mepother mri

Abstract

Aims Transcranial focus ultrasound stimulation (tFUS) is a promising non-invasive neuromodulation technology. This study aimed to evaluate the modulatory effects of tFUS on human motor cortex (M1) excitability and explore the mechanism of neurotransmitter-related intracortical circuitry and plasticity. Methods Single pulse transcranial magnetic stimulation (TMS)-eliciting motor-evoked potentials (MEPs) were used to assessed M1 excitability in 10 subjects. Paired-pulse TMS was used to measure the effects of tFUS on GABA- and glutamate-related intracortical excitability and 1 H-MRS was used to assess the effects of repetitive tFUS on GABA and Glx (glutamine + glutamate) neurometabolic concentrations in the targeting region in nine subjects. Results The etFUS significantly increased M1 excitability, decreased short interval intracortical inhibition (SICI) and long interval intracortical inhibition (LICI). The itFUS significantly suppressed M1 excitability, increased SICI, LICI, and decreased intracortical facilitation (ICF). Seven times of etFUS decreased the GABA concentration (6.32%), increased the Glx concentration (12.40%), and decreased the GABA/Glx ratio measured by MRS, while itFUS increased the GABA concentration (18.59%), decreased Glx concentration (0.35%), and significantly increased GABA/Glx ratio. Conclusion The findings support that tFUS with different parameters can exert excitatory and inhibitory neuromodulatory effects on the human motor cortex. We provide novel insights that tFUS change cortical excitability and plasticity by regulating excitatory-inhibition balance related to the GABAergic and glutamatergic receptor function and neurotransmitter metabolic level.

Abstract via europepmc.

Specieshuman
Subjects10 participants
Sessions per subject2, 3, 7swept
Randomisedyes
Blindingnot reported
Sham / controlundescribed
Auditory controlnot reported
Readout timingoffline
Anaesthesianot applicable
Readoutsemg mep, other mriSingle- and paired-pulse TMS-elicited MEP (SICI, LICI, ICF); 1H-MRS (MEGA-PRESS) GABA and Glx concentrations
Direction of effectbidirectionaletFUS (higher duty cycle/PRF) significantly increased MEP amplitude and reduced SICI and LICI; itFUS (lower duty cycle/PRF) significantly decreased MEP amplitude, increased SICI and LICI, and decreased ICF. Seven days of etFUS decreased the GABA/Glx ratio (not significant), while itFUS significantly increased the GABA/Glx ratio.
Adverse eventsnone observedDuring the study, no adverse effects were spontaneously reported or after questioning the subjects post each stimulation, supporting the safety profile of the current pulsing schemes.

Exposures

Exposure 1: etFUS / itFUS to left M1

Target: primary motor cortex — “left M1 (hand motor cortex)
Device: custom-built · GreenValley BrainTech Medical Techology Corportion

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)0.2, 0.4swept✓✓
Pulse repetition frequency (Hz)2,000, 50swept✓✓
Duty cycle (%)40, 2swept✓✓
Sonication duration (s)0.5✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)not reported
In-situ estimatemeasurementmean or range across subjects
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)0.616, 2.46swept✓✓
In-situ Ispta (W/cm²)0.00308, 0.0123swept✓✓
Protocol, in the paper’s words

Two parameter sets were used: etFUS (pulse width T1=200 microseconds, pulse-repetition period T2=0.5 ms, burst duration T3=500 ms, burst period T4=2 s, PRF=2000 Hz, DC=40%) produced excitatory effects; itFUS (T1=400 microseconds, T2=20 ms, T3=500 ms, T4=2 s, PRF=50 Hz, DC=2%) produced inhibitory effects. Each was applied for 5 min in Experiments 1 and 2 (with sham in Experiment 1), and 5 min once daily for 7 consecutive days in Experiment 3.

Flags from extraction

  • n_sessions_per_subjectSession counts differ across the three experiments (up to 3 sessions in Exp 1, up to 2 in Exp 2, 7 consecutive days in Exp 3); a single count could not be given.
  • sham_typeThe mechanism of the sham condition (e.g., power off, transducer angled away) is not described in the text.
  • exposures[0].in_situ.reported_asISPPA/ISPTA are reported as a min-max range from spatial scanning of the acoustic field through a skull fragment, not as a range across subjects; 'mean_or_range_across_subjects' is the closest available category.
  • exposures[0].in_situ.isppa_w_cm2Reported as a single measured range without specifying whether it corresponds to the etFUS condition, itFUS condition, or both.