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High resolution ultrasonic neural modulation observed via in vivo two-photon calcium imaging

Zongyue Cheng, Chenmao Wang, Bowen Wei, Wenbiao Gan, Qifa Zhou, Meng Cui

Brain Stimulation 2022, 15, 190-196 · 10.1016/j.brs.2021.12.005

rodenthealthycellular imagingeeg meg

Abstract

Neural modulation plays a major role in delineating the circuit mechanisms and serves as the cornerstone of neural interface technologies. Among the various modulation mechanisms, ultrasound enables noninvasive label-free deep access to mammalian brain tissue. To date, most if not all ultrasonic neural modulation implementations are based on ∼1 MHz carrier frequency. The long acoustic wavelength results in a spatially coarse modulation zone, often spanning over multiple function regions. The modulation of one function region is inevitably linked with the modulation of its neighboring regions. Moreover, the lack of in vivo cellular resolution cell-type-specific recording capabilities in most studies prevents the revealing of the genuine cellular response to ultrasound. To significantly increase the spatial resolution, we explored the application of high-frequency ultrasound. To investigate the neuronal response at cellular resolutions, we developed a dual-modality system combining in vivo two-photon calcium imaging and focused ultrasound modulation. The studies show that the ∼30 MHz ultrasound can suppress the neuronal activity in awake mice at 100-μm scale spatial resolutions, paving the way for high-resolution ultrasonic neural modulation. The dual-modality in vivo system validated through this study will serve as a general platform for studying the dynamics of various cell types in response to ultrasound.

Abstract via europepmc.

Speciesmouse (C57BL/6)
Subjectsnot reported animals
Sessions per subjectnot reported
Randomisedno
Blindingnone
Sham / controlactive control site
Auditory controlnot reported
Readout timingonline
Anaesthesiaboth
Readoutscellular imaging, eeg megin vivo two-photon calcium imaging (GCaMP6s); EEG recording with wavelet decomposition
Direction of effectinhibitory30 MHz ultrasound reliably suppressed calcium transients and increased low-frequency (0.3-1.3 Hz) EEG activity in awake mice; both effects disappeared under isoflurane anesthesia.
Adverse eventsnone observedAlthough much stronger ultrasound (Ispta reached 11.8 W/cm2, CW) was employed in this control study, no microglia aggregation was observed. Brain tissue temperature variation during ultrasound modulation showed less than 1 C variation and negligible difference between awake and anesthetized mice.

Exposures

Exposure 1: 30 MHz (also 20 and 40 MHz) ultrasound to visual cortex

Target: primary visual cortex — “visual cortex (V1)
Device: Olympus / Panametrics · Olympus NDT · PI35-2-R0.50

Pulse timing
Waveformcontinuous
Fundamental frequency (kHz)20,000, 30,000, 40,000swept✓✓
Pulse duration (ms)not applicable
Pulse repetition frequency (Hz)not applicable
Duty cycle (%)100?
Sonication duration (s)60✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)2.17, 4.46swept?
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

The typical recording session was 300 s long: the first 60 s the ultrasound was off (baseline), the next 60 s the ultrasound was on (modulation), and the last 180 s the ultrasound was off (recovery). Amplitude-modulated (pulsed) waveforms were also tested at a 10% duty cycle with modulation frequency varied from 100 Hz to 100 kHz, and with sinusoidal amplitude modulation from 0.5 to 2 MHz, but none of these modulated waveforms suppressed calcium transients as effectively as the CW signal.

Consistency checks: f0 out of range.

Exposure 2: ultrasound to motor cortex (parameters not restated)

Target: motor cortex — “motor cortex
Device: Olympus / Panametrics · Olympus NDT · PI35-2-R0.50

Pulse timing
Waveformnot reported
Fundamental frequency (kHz)not reported
Pulse duration (ms)not reported
Pulse repetition frequency (Hz)not reported
Duty cycle (%)not reported
Sonication duration (s)not reported
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
Protocol, in the paper’s words

We also tested the motor cortex which showed the same effects (Supplementary Fig. 5).

Flags from extraction

  • n_subjects4 mice specifically reported for the primary calcium-suppression phenomenon ('the statistics of 4 mice and 180 neurons'); additional, unspecified numbers of mice ('at least three mice ... in each experiment') were used in other sub-experiments (frequency comparisons, motor cortex, transgenic controls) not included in this count.
  • exposures[0].fundamental_frequency_khz20 and 40 MHz were also tested at the same target as the primary 30 MHz condition, with only a qualitative comparison of suppression strength reported (no separate intensity/timing values); combined into a single exposure per the frequency-sweep rule.
  • exposures[0].free_field.ispta_w_cm2Intensity was measured with a hydrophone 'at the sound focus', typically a free-field/water measurement technique, but mice had a cranial window (skull removed, plastic coverslip with ~90% acoustic transmission) rather than an intact skull, so domain assignment (free-field vs. delivered-at-brain) is uncertain.
  • exposures[0].timing.duty_cycle_pctA pulsed/amplitude-modulated condition at 10% duty cycle and modulation-frequency range 100 Hz-100 kHz is also described in text, but was a secondary comparison to the primary CW protocol; not entered as separate list values to avoid conflating with the CW dose-response data.
  • exposures[1].fundamental_frequency_khzMotor cortex is mentioned only briefly in Methods with reference to a supplementary figure; no frequency, intensity, or timing values were restated for this target, so it is recorded as not_reported rather than assumed identical to the visual cortex protocol.
  • sham_typeNo sham condition is described; the closest control is moving the ultrasound transducer 5 mm away from the imaging/recording site, coded as 'other'.