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Improved Anatomical Specificity of Non-invasive Neuro-stimulation by High Frequency (5 MHz) Ultrasound

Guo-Feng Li, Hui-Xia Zhao, Hui Zhou, Fei Yan, Jing-Yao Wang, Chang-Xi Xu, Cong-Zhi Wang, Li-Li Niu, Long Meng, Song Wu, Huai-Ling Zhang, Wei-Bao Qiu, Hai-Rong Zheng

Scientific Reports 2016, 6 · 10.1038/srep24738

rodenthealthyemg mepbehaviourhistology molecular

Abstract

Low frequency ultrasound (<1 MHz) has been demonstrated to be a promising approach for non-invasive neuro-stimulation. However, the focal width is limited to be half centimeter scale. Minimizing the stimulation region with higher frequency ultrasound will provide a great opportunity to expand its application. This study first time examines the feasibility of using high frequency (5 MHz) ultrasound to achieve neuro-stimulation in brain, and verifies the anatomical specificity of neuro-stimulation in vivo. 1 MHz and 5 MHz ultrasound stimulation were evaluated in the same group of mice. Electromyography (EMG) collected from tail muscles together with the motion response videos were analyzed for evaluating the stimulation effects. Our results indicate that 5 MHz ultrasound can successfully achieve neuro-stimulation. The equivalent diameter (ED) of the stimulation region with 5 MHz ultrasound (0.29 ± 0.08 mm) is significantly smaller than that with 1 MHz (0.83 ± 0.11 mm). The response latency of 5 MHz ultrasound (45 ± 31 ms) is also shorter than that of 1 MHz ultrasound (208 ± 111 ms). Consequently, high frequency (5 MHz) ultrasound can successfully activate the brain circuits in mice. It provides a smaller stimulation region, which offers improved anatomical specificity for neuro-stimulation in a non-invasive manner.

Abstract via europepmc.

Speciesmouse (C57BL/6)
Subjects10 animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlnone
Auditory controlnot reported
Readout timingonline
Anaesthesiaanaesthetised
Readoutsemg mep, behaviour, histology molecularEMG signals from tail muscles; video-recorded tail-flick/motion responses; hematoxylin-eosin (HE) staining of brain slices for safety
Direction of effectexcitatoryBoth 1 MHz and 5 MHz ultrasound evoked EMG-recorded tail-flick motor responses; peak EMG amplitude increased with acoustic intensity, and 5 MHz produced a smaller, more anatomically specific activation region with shorter response latency than 1 MHz.
Adverse eventsnone observedPeak brain temperature elevation was 0.2°C for 1 MHz (300 ms stimulus) and 1.6°C for 5 MHz (300 ms stimulus), decreasing to 0.8°C for 5 MHz at 150 ms; HE staining showed no morphological damage, bleeding, or necrosis versus control mice.

Exposures

Exposure 1: 1 MHz ultrasound stimulation of mouse brain (tail-flick evoking site)

Target: other — “3.5 mm lateral to the midline and 7.5 mm posterior to the rear corner of mouse eyes
Device: Olympus / Panametrics · Olympus NDT · V314-1 MHz

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)1,000✓✓
Pulse duration (ms)0.5✓✓
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)50pulse duration × PRF gives 50%✓✓
Sonication duration (s)0.3✓✓
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 estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Ispta, domain unspecified (W/cm²)0.13, 0.23swept?
Protocol, in the paper’s words

All parameters were kept consistent between frequencies (50% duty cycle of pulse, 1 ms pulse period, 1 kHz pulse repetition frequency, 300 pulses per stimulus, and 3 second interval); for 1 MHz, cycles-per-pulse (CPP) was set to 500 to give a 0.5 ms pulse duration. Acoustic intensity was varied over six Ispta values from 130 to 230 mW/cm2, delivered for a stimulation duration of one minute per intensity/site; nine stimulation sites 0.3 mm apart were tested per mouse for the anatomical-specificity comparison.

Exposure 2: 5 MHz ultrasound stimulation of mouse brain (tail-flick evoking site)

Target: other — “3.5 mm lateral to the midline and 7.5 mm posterior to the rear corner of mouse eyes
Device: Olympus / Panametrics · Olympus NDT · V308-5 MHz

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)5,000✓✓
Pulse duration (ms)0.5✓✓
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)50pulse duration × PRF gives 50%✓✓
Sonication duration (s)0.3✓✓
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 estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Ispta, domain unspecified (W/cm²)0.13, 0.23swept?
Protocol, in the paper’s words

Same block structure as the 1 MHz condition (50% duty cycle, 1 ms pulse period, 1 kHz PRF, 300 pulses per stimulus, 3 s interval); for 5 MHz, CPP was set to 2500 to give the same 0.5 ms pulse duration, with driving amplitude increased to compensate for the ~4.2 dB skull attenuation at 5 MHz. Acoustic intensity was varied over six Ispta values from 130 to 230 mW/cm2, one minute per intensity/site; for the safety/HE-stain cohort, 5 MHz was also delivered continuously for 30 minutes.

Flags from extraction

  • n_subjectsPaper reports several different n values across analyses (n=5, n=6, n=10, n=20 for HE stain safety group); n_subjects taken from the main Animal preparation paragraph.
  • exposures[0].target.termsPaper never names the stimulated brain region anatomically; it is identified only by stereotaxic coordinates and by the tail-flick motor response it evokes.
  • exposures[0].unspecified_domain.ispta_w_cm2Paper does not state whether these Ispta values are free-field or in-brain; they are described only as 'compensated' to offset skull attenuation, so domain is ambiguous and placed in unspecified_domain.
  • exposures[1].unspecified_domain.ispta_w_cm2Same ambiguity as exposures[0]; both frequencies were driven to the same compensated intensity level.
  • exposures[0].timing.sonication_duration_s300 ms stimulus duration is taken from the temperature-safety section (same protocol); the main neuromodulation Methods describe the train as '300 pulses per stimulus' at 1 kHz PRF without directly stating its length in ms, so this reuses the safety-section figure for the same protocol.
  • exposures[1].timing.sonication_duration_sSame as exposures[0]; 5 MHz was also tested at a shorter 150 ms duration for thermal safety, noted in protocol_description.