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Neuromodulatory Responses Elicited by Intermittent versus Continuous Transcranial Focused Ultrasound Stimulation of the Motor Cortex in Rats

Tsung-Hsun Hsieh, Po-Chun Chu, Thi Xuan Dieu Nguyen, Chi-Wei Kuo, Pi-Kai Chang, Kai-Hsiang Stanley Chen, Hao-Li Liu

International Journal of Molecular Sciences 2024, 25, 5687 · 10.3390/ijms25115687

rodenthealthyemg mephistology molecular

Abstract

Transcranial focused ultrasound stimulation (tFUS) has emerged as a promising neuromodulation technique that delivers acoustic energy with high spatial resolution for inducing long-term potentiation (LTP)- or depression (LTD)-like plasticity. The variability in the primary effects of tFUS-induced plasticity could be due to different stimulation patterns, such as intermittent versus continuous, and is an aspect that requires further detailed exploration. In this study, we developed a platform to evaluate the neuromodulatory effects of intermittent and continuous tFUS on motor cortical plasticity before and after tFUS application. Three groups of rats were exposed to either intermittent, continuous, or sham tFUS. We analyzed the neuromodulatory effects on motor cortical excitability by examining changes in motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS). We also investigated the effects of different stimulation patterns on excitatory and inhibitory neural biomarkers, examining c-Fos and glutamic acid decarboxylase (GAD-65) expression using immunohistochemistry staining. Additionally, we evaluated the safety of tFUS by analyzing glial fibrillary acidic protein (GFAP) expression. The current results indicated that intermittent tFUS produced a facilitation effect on motor excitability, while continuous tFUS significantly inhibited motor excitability. Furthermore, neither tFUS approach caused injury to the stimulation sites in rats. Immunohistochemistry staining revealed increased c-Fos and decreased GAD-65 expression following intermittent tFUS. Conversely, continuous tFUS downregulated c-Fos and upregulated GAD-65 expression. In conclusion, our findings demonstrate that both intermittent and continuous tFUS effectively modulate cortical excitability. The neuromodulatory effects may result from the activation or deactivation of cortical neurons following tFUS intervention. These effects are considered safe and well-tolerated, highlighting the potential for using different patterns of tFUS in future clinical neuromodulatory applications.

Abstract via europepmc.

Speciesrat (Sprague-Dawley)
Subjects7, 8swept animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlinactive transducer
Auditory controlnot reported
Readout timingoffline
Anaesthesiaanaesthetised
Readoutsemg mep, histology molecularc-Fos, GAD-65 and GFAP immunohistochemistry; motor-evoked potentials (MEPs) via TMS
Direction of effectbidirectionalIntermittent tFUS facilitated MEP amplitude (significant only 0-5 min post-stimulation), while continuous tFUS suppressed MEP amplitude for the full 30 min post-stimulation; intermittent tFUS increased c-Fos and did not increase GAD-65, continuous tFUS decreased c-Fos and increased GAD-65.
Adverse eventsnone observedNo obvious astrogliosis (GFAP) was observed at or near the sonicated sites at 1, 3, or 7 days after either continuous or intermittent tFUS compared with sham.

Exposures

Exposure 1: Intermittent vs continuous tFUS to right primary motor cortex

Target: primary motor cortex — “right primary motor cortex
Device: other named manufacturer · NepaGene · SonoPore KTAC-4000

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)1,000✓✓
Pulse duration (ms)not reported
Pulse repetition frequency (Hz)not reported
Duty cycle (%)30, 8swept✓✓
Sonication duration (s)30, 600swept✓✓
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 estimatemeasurementsingle value
In-situ pressure (kPa)137✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)0.188, 0.0469swept✓✓
Protocol, in the paper’s words

Intermittent transcranial tFUS: 30 s ultrasound trains (30% duty cycle) followed by 90 s rest periods, repeated five times for a total duration of 600 s. Continuous tFUS: same pressure at an 8% duty cycle for a continuous duration of 600 s. Both delivered as a single 600 s intervention under anaesthesia.

Flags from extraction

  • n_subjectsGroup sizes (7-8 rats per group) are stated only in the Figure 1 legend, not in main text or a table, so per the three-way rule this is recorded as not_reported.
  • exposures[0].in_situ.ispta_w_cm2List order is [intermittent, continuous] matching duty_cycle_pct and sonication_duration_s list order.
  • exposures[0].timing.pulse_duration_msNo pulse repetition frequency or intra-train pulse duration is stated, only the overall duty cycle of each protocol, so the burst rule cannot be resolved; both durations (30 s train and 600 s continuous) are given in protocol_description.
  • exposures[0]Intermittent and continuous protocols are treated as one exposure (same target and frequency) with timing parameters as lists, per the one-exposure-per-target-frequency rule.