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Transcranial ultrasound stimulation selectively affects cortical neurovascular coupling across neuronal types and LFP frequency bands

Zhaocheng Su, Mengyang Liu, Yi Yuan, Honglei Jiao

Cerebral Cortex 2024 · 10.1093/cercor/bhad465

rodenthealthyinvasive electrophysiologycerebral haemodynamics

Abstract

Previous studies have affirmed that transcranial ultrasound stimulation (TUS) can influence cortical neurovascular coupling across low-frequency (0-2 Hz)/high-frequency (160-200 Hz) neural oscillations and hemodynamics. Nevertheless, the selectivity of this coupling triggered by transcranial ultrasound stimulation for spike activity (> 300 Hz) and additional frequency bands (4-150 Hz) remains elusive. We applied transcranial ultrasound stimulation to mice visual cortex while simultaneously recording total hemoglobin concentration, spike activity, and local field potentials. Our findings include (1) a significant increase in coupling strength between spike firing rates of putative inhibitory neurons/putative excitatory neurons and total hemoglobin concentration post-transcranial ultrasound stimulation; (2) an ~ 2.1-fold higher Pearson correlation coefficient between putative inhibitory neurons and total hemoglobin concentration compared with putative excitatory neurons and total hemoglobin concentration (*P < 0.05); (3) a notably greater cross-correlation between putative inhibitory neurons and total hemoglobin concentration than that between putative excitatory neurons and total hemoglobin concentration (*P < 0.05); (4) an enhancement of Pearson correlation coefficient between the relative power of γ frequency band (30-80 Hz), hγ frequency band (80-150 Hz) and total hemoglobin concentration following transcranial ultrasound stimulation (*P < 0.05); and (5) strongest cross-correlation observed at negative delay for θ frequency band, and positive delay for α, β, γ, hγ frequency bands. Collectively, these results demonstrate that cortical neurovascular coupling evoked by transcranial ultrasound stimulation exhibits selectivity concerning neuronal types and local field potential frequency bands.

Abstract via europepmc.

Speciesmouse (C57BL/6)
Subjects18 animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlnone
Auditory controlnot reported
Readout timingboth
Anaesthesiaawake
Readoutsinvasive electrophysiology, cerebral haemodynamics — Multi-channel silicon electrode spikes and LFP; intrinsic optical signal imaging of HbT
Direction of effectexcitatoryTUS increased the firing rate of putative inhibitory and excitatory neurons and HbT, and increased neurovascular coupling strength; relative gamma power increased and alpha power decreased.
Adverse eventsnot reported

Exposures

Exposure 1: TUS of mouse visual cortex

Target: primary visual cortex — “visual cortex”
Device: Olympus / Panametrics · Olympus · V323-SU ✓

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓✓
Pulse duration (ms)not reportedimplied by duty cycle ÷ PRF: 0.5 ms (not stated by the paper)⚑
Pulse repetition frequency (Hz)1,000✓✓✓
Duty cycle (%)50✓✓✓
Sonication duration (s)0.7✓✓✓
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
Pressure, domain unspecified (kPa)450✓✓✓⚑
Isppa, domain unspecified (W/cm²)6.75✓✓✓
Protocol, in the paper’s words

Stimulation duration 700 ms, PRF 1 kHz, duty cycle 50%; ultrasound stimulation at 10-s intervals and the mean over eight trials was computed.

Flags from extraction

  • n_subjects — 18 mice were used but analyses report n = 8 mice; enrolled number recorded.
  • exposures[0].unspecified_domain.pressure_kpa — Pressure (~0.45 MPa) and Isppa given without stating the domain.
  • anaesthesia — Surgery under isoflurane, recovery for 3 d; recording described as in conscious/awake mice.
  • exposures[0].timing.pulse_duration_ms — Pulse duration not stated; not computed from DC and PRF.