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Mechanisms of theta burst transcranial ultrasound induced plasticity in the human motor cortex

Yazan Shamli Oghli, Talyta Grippe, Tarun Arora, Tasnuva Hoque, Ghazaleh Darmani, Robert Chen

Brain Stimulation 2023, 16, 1135-1143 · 10.1016/j.brs.2023.07.056

human healthyhealthyemg mep

Abstract

Background Transcranial ultrasound stimulation (TUS) is a novel non-invasive brain stimulation technique with high depth penetrance and spatial resolution. Theta-burst TUS (tbTUS) is a plasticity-inducing protocol which increases motor cortical excitability for up to 30 min following 80s of sonication. While this protocol may have therapeutic potential for the treatment of psychiatric and neurological disorders, the mechanisms of action of TUS remain unclear. Objective We conducted the first pharmacological study to examine the mechanisms of TUS in human primary motor cortex. By administering brain-active drugs with known mechanisms of action, we aimed to elucidate the mechanisms of tbTUS. Methods Fourteen healthy subjects participated in a within-subjects randomized, double-blind, cross-over study with five visits. At each visit, one of four study drugs (carbamazepine - Na + channel blocker, nimodipine - L-type Ca 2+ channel blocker, lorazepam - positive allosteric modulator of gamma-aminobutyric acid (GABA) type A receptor, dextromethorphan - N-methyl-d-aspartate receptor antagonist) or placebo was administered in random order, followed by tbTUS. Results The plasticity effects of tbTUS on motor cortex excitability measured by motor-evoked potential amplitudes elicited by transcranial magnetic stimulation were reduced by all study drugs compared to placebo. Conclusion tbTUS may induce NMDA-dependent synaptic plasticity since the effects are blocked by increased GABA A receptor activities and voltage-gated Na + and Ca 2+ channels blockers. These results are consistent with the hypotheses that tbTUS induced long-term potentiation-like mechanisms and that TUS involves activation of mechanosensitive Na + and Ca 2+ channels. Alternatively, non-specific pharmacologically induced changes in excitatory/inhibitory balance might have interfered with the effects of tbTUS.

Abstract via europepmc.

Specieshuman
Subjects16 participants
Sessions per subject5
Randomisedyes
Blindingdouble
Sham / controlnone
Auditory controlnot reported
Readout timingoffline
Anaesthesianot applicable
Readoutsemg mepmotor evoked potential (MEP) amplitude; short-interval intracortical inhibition (SICI); intracortical facilitation (ICF); resting motor threshold (RMT); SI1mV
Direction of effectexcitatoryIn the placebo condition, tbTUS increased MEP amplitude relative to pre-tbTUS baseline for up to 60 min post-stimulation; this facilitatory effect was reduced/eliminated by carbamazepine, nimodipine, and dextromethorphan, and by lorazepam at 30 and 60 (but not 5) minutes post-tbTUS.
Adverse eventsobservedThe same subject also reported mild itchiness for NDP, CBZ and DXT, particularly over the scalp area where the TUS transducer was placed. There were no unexpected side effects when administering TUS and drugs together.

Exposures

Exposure 1: theta-burst TUS (tbTUS) to left M1

Target: primary motor cortex — “left M1 (FDI hotspot)
Device: Sonic Concepts · Sonic Concepts Inc. · custom 2-channel annular array transducer

Pulse timing
Waveformtheta burst
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)20✓✓
Pulse repetition frequency (Hz)5✓✓
Duty cycle (%)10pulse duration × PRF gives 10%✓✓
Sonication duration (s)80✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)11.73✓✓
Free-field Ispta (W/cm²)1.17✓✓
In-situ estimatederatingsingle value
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)2.93✓✓
In-situ Ispta (W/cm²)0.29✓✓
Protocol, in the paper’s words

As with Zeng et al. [7], an 80s sonication with tone burst duration of 20 ms, 5Hz PRF, 10% duty cycle and 20W intensity was delivered. Sonication depth was set to 30 mm to approximate the scalp-to-cortex distance of the M1. One tbTUS delivery occurred per visit, after a 2.5 h drug/placebo wait period, at each of five study visits.

Flags from extraction

  • n_subjects16 subjects enrolled; 2 dropped out after visit 1 and are excluded from most analyses (14 analysed for most drugs, 13 for LRZ/DXT). n_subjects reported here is the enrolled total.
  • exposures[0].timing.pulse_duration_msPaper calls this a 'tone burst duration' of 20 ms within an 80 s train; consistent with duty cycle (10%) / PRF (5 Hz) = 20 ms, so no arithmetic conflict, but confirming burst-rule resolution here for transparency.
  • sham_typeStudy tested drug x tbTUS only; no sham/control tbTUS condition was included (explicitly noted as a limitation).