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Selective manipulation of excitatory and inhibitory neurons in top-down and bottom-up visual pathways using ultrasound stimulation

Yehhyun Jo, Xiaojia Liang, Hong Hanh Nguyen, Yeonseo Choi, Minji Choi, Ga-Eun Bae, Yakdol Cho, Jiwan Woo, Hyunjoo Jenny Lee

Brain Stimulation 2025, 18, 848-862 · 10.1016/j.brs.2025.04.008

rodenthealthyinvasive electrophysiologyhistology molecular

Abstract

Introduction Techniques for precise manipulation of neurons in specific neural pathways are crucial for excitatory/inhibitory (E/I) balance and investigation of complex brain circuits. Low-intensity focused ultrasound stimulation (LIFUS) has emerged as a promising tool for noninvasive deep-brain targeting at high spatial resolution. However, there is a lack of studies that extensively investigate the modulation of top-down and bottom-up corticothalamic circuits via selective manipulation of excitatory and inhibitory neurons. Here, a comprehensive methodology using electrophysiological recording and c-Fos staining is employed to demonstrate pulse repetition frequency (PRF)-dependent E/I selectivity of ultrasound stimulation in the top-down and bottom-up corticothalamic pathways of the visual circuit in rodents. Materials and methods Ultrasound stimulation at various PRFs is applied to either the lateral posterior nucleus of the thalamus (LP) or the primary visual cortex (V1), and multi-channel single-unit activity is recorded from the V1 using a silicon probe. Results and conclusion Our results demonstrate that high-frequency PRFs, particularly at 3 kHz and 1 kHz, are effective at activating the bidirectional corticothalamic visual pathway. In addition, brain region-specific PRFs modulate E/I cortical signals, corticothalamic projections, and synaptic neurotransmission, which is imperative for circuit-specific applications and behavioral studies.

Abstract via europepmc.

Speciesmouse
Subjects61 animals
Sessions per subject1
Randomisedyes
Blindingnot reported
Sham / controlinactive transducer, active control site, other
Auditory controlcontrol experiment
Readout timingboth
Anaesthesiaanaesthetised
Readoutsinvasive electrophysiology, histology molecularextracellular single-/multi-unit and LFP recording via silicon probe with Kilosort spike sorting and FSU/RSU classification; c-Fos immunohistochemistry co-stained with vGLUT1 (glutamatergic) and GABA (GABAergic) markers
Direction of effectexcitatoryLIFUS of either the LP or V1 significantly increased V1 single-unit firing rates and brain-wide c-Fos activation across the LP-V1 circuit relative to sham/control; PRFs of 3 kHz and 1 kHz most effectively increased firing of FSU, RSU1 and RSU2 units and preferentially activated glutamatergic (vGLUT1+) rather than GABAergic neurons, with region- and PRF-dependent selectivity.
Adverse eventsnone observedMechanical index (0.55) and thermal dose (0.04 CEM) were below the MI cavitation threshold (1.9) and thermal dose threshold (1 CEM); a thermocouple/brain-phantom test showed an instantaneous peak temperature change of ~1.27C during the stimulation protocol, and H&E-stained brain sections showed no structural damage post-stimulation.

Exposures

Exposure 1: LIFUS of the lateral posterior thalamic nucleus (LP), recording from V1 (LP-V1 group)

Target: thalamus — “lateral posterior nucleus of the thalamus (LP)
Device: other named manufacturer · Hagisonic Inc.

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)5,000✓✓
Pulse duration (ms)not reported
Pulse repetition frequency (Hz)3,000, 1,000, 80swept✓✓
Duty cycle (%)50✓✓
Sonication duration (s)1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)1,240✓✓
Free-field Isppa (W/cm²)51.25✓✓
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

The first function generator delivered a square wave at PRFs of 3 kHz, 1 kHz, and 80 Hz, corresponding to 3000 cycles, 1000 cycles, and 80 cycles for a total pulse train of 1 s, all at a 50% duty cycle. The first function generator was controlled using a custom MATLAB program to generate 20-min stimulation sessions with an inter-stimulation interval (ISI) of 10 s. Three different PRF conditions of 3 kHz, 1 kHz, and 80 Hz were applied in a random sequence, each lasting 20 min. Sham conditions included SHAM-AG (air gap between collimator and brain), SHAM-OT (off-target transcranial site, to check bone-conduction auditory activation), and SHAM-PS (direct stimulation of the probe shank, to check vibration-induced activation).

Exposure 2: LIFUS of the primary visual cortex (V1), recording from V1 (V1-V1 group)

Target: primary visual cortex — “primary visual cortex (V1)
Device: other named manufacturer · Hagisonic Inc.

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)5,000✓✓
Pulse duration (ms)not reported
Pulse repetition frequency (Hz)3,000, 1,000, 80swept✓✓
Duty cycle (%)50✓✓
Sonication duration (s)1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)1,240✓✓
Free-field Isppa (W/cm²)51.25✓✓
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

The first function generator delivered a square wave at PRFs of 3 kHz, 1 kHz, and 80 Hz, corresponding to 3000 cycles, 1000 cycles, and 80 cycles for a total pulse train of 1 s, all at a 50% duty cycle. The first function generator was controlled using a custom MATLAB program to generate 20-min stimulation sessions with an inter-stimulation interval (ISI) of 10 s. Three different PRF conditions of 3 kHz, 1 kHz, and 80 Hz were applied in a random sequence, each lasting 20 min. Sham conditions included SHAM-AG (air gap between collimator and brain), SHAM-OT (off-target transcranial site, to check bone-conduction auditory activation), and SHAM-PS (direct stimulation of the probe shank, to check vibration-induced activation).

Flags from extraction

  • n_subjects61 is the total mice used across the whole study (electrophysiology, c-Fos IHC, neurotransmitter co-staining, and sham/control groups); not all received active ultrasound. Primary electrophysiology cohorts were n=12 (LP-V1 group) and n=8 (V1-V1 group), reported in separate sentences.
  • exposures[0].target.termsThe paper's target is the 'lateral posterior nucleus (LP) of the thalamus'; no exact match exists in the target vocabulary (closest concepts are pulvinar or posterior_thalamic_nucleus), so the parent term 'thalamus' is used.
  • auditory_controlSHAM-OT (ultrasound aimed transcranially at an off-target site) was used specifically to test for bone-conduction auditory confounds, but does not match any listed auditory_control vocabulary term exactly; classified as other.
  • exposures[0].timing.pulse_duration_msDuty cycle (50%) and PRF (3/1 kHz/80 Hz) are stated but individual pulse width in ms is not stated by the paper; left not_reported rather than computed.
  • exposures[1].timing.pulse_duration_msSame as exposures[0]: pulse width not explicitly stated.
  • exposures[0].in_situ.methodCraniotomy removed the skull over the target for the actual in vivo experiments, but the paper does not explicitly relabel the hydrophone-measured free-field values as in-situ brain values for this preparation.
  • exposures[1].in_situ.methodSame as exposures[0].