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Transcranial ultrasound neuromodulation of the thalamic visual pathway in a large animal model and the dose-response relationship with MR-ARFI

Morteza Mohammadjavadi, Ryan T. Ash, Ningrui Li, Pooja Gaur, Jan Kubanek, Yamil Saenz, Gary H. Glover, Gerald R. Popelka, Anthoney M. Norcia, Kim Butts Pauly

Scientific Reports 2022, 12 · 10.1038/s41598-022-20554-4

large animalhealthyeeg megother mri

Abstract

Neuromodulation of deep brain structures via transcranial ultrasound stimulation (TUS) is a promising, but still elusive approach to non-invasive treatment of brain disorders. The purpose of this study was to confirm that MR-guided TUS of the lateral geniculate nucleus (LGN) can modulate visual evoked potentials (VEPs) in the intact large animal; and to study the impact on cortical brain oscillations. The LGN on one side was identified with T2-weighted MRI in sheep (all male, n = 9). MR acoustic radiation force imaging (MR-ARFI) was used to confirm localization of the targeted area in the brain. Electroencephalographic (EEG) signals were recorded, and the visual evoked potential (VEP) peak-to-peak amplitude (N70 and P100) was calculated for each trial. Time-frequency spectral analysis was performed to elucidate the effect of TUS on cortical brain dynamics. The VEP peak-to-peak amplitude was reversibly suppressed relative to baseline during TUS. Dynamic spectral analysis demonstrated a change in cortical oscillations when TUS is paired with visual sensory input. Sonication-associated microscopic displacements, as measured by MR-ARFI, correlated with the TUS-mediated suppression of visual evoked activity. TUS non-invasively delivered to LGN can neuromodulate visual activity and oscillatory dynamics in large mammalian brains.

Abstract via europepmc.

Speciessheep
Subjects9 animals
Sessions per subject1, 2swept
Randomisednot reported
Blindingsingle
Sham / controlinactive transducer, active control site
Auditory controlnone
Readout timingboth
Anaesthesiaanaesthetised
Readoutseeg meg, other mriVisual evoked potentials (VEP) via scalp EEG; MR acoustic radiation force imaging (MR-ARFI) microscopic tissue displacement
Direction of effectinhibitoryUnilateral TUS of the LGN reversibly suppressed binocular visual evoked potential (VEP) peak-to-peak amplitude by almost 50% relative to baseline, recovering during subsequent non-LGN control sonication; TUS also modulated light-elicited cortical oscillations, increasing non-phase-locked upper-beta/gamma power and a smaller phase-locked theta/alpha increase.
Adverse eventsnot reportedUltrasound parameters were within the FDA-approved safety limit for Isppa (<190 W/cm2) but exceeded the Ispta limit (<720 mW/cm2) due to the high sonication repetition rate; bioheat simulation estimated a temperature rise of 1.3 +/- 0.9 degC at the LGN; the paper cites a companion histological study finding no evidence of microscopic tissue injury in these sheep even with longer sonication durations and multiple days of treatment.

Exposures

Exposure 1: MR-guided TUS of the lateral geniculate nucleus (LGN), with non-LGN (medial putamen/internal capsule) active control sonication

Target: lateral geniculate nucleus — “lateral geniculate nucleus (LGN) of the thalamus, unilateral
Device: Insightec · Insightec Ltd. · ExAblate 2100 (1024-element phased array)

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)550✓✓
Pulse duration (ms)1✓✓
Pulse repetition frequency (Hz)500✓✓
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 estimatemeasurementmean or range across subjects
In-situ pressure (kPa)550, 1,000swept✓✓
In-situ Isppa (W/cm²)19.3, 63.8swept✓✓
In-situ Ispta (W/cm²)2.8, 9.57swept✓✓
Protocol, in the paper’s words

Nine male sheep (6 LGN-TUS experiments on 5 animals; 5 sham experiments on 4 animals, including one animal given zero TUS intensity and three 'Active Sham' animals where the transducer was unintentionally off-target due to movement) underwent a 5-min light-only EEG baseline, then two 20-min LGN sonication blocks, then three 20-min non-LGN control-site sonication blocks (control site ~10 mm anterior to LGN, spanning medial putamen and adjacent internal capsule). Each 20-min block cycled four interleaved 15 s conditions every minute: no stimulus, light-only, TUS-only, and light-plus-TUS (1 Hz repetition). Pulse trains had a rectangular envelope, repeated once per second.

Flags from extraction

  • blindingBlinding was incidental rather than a designed protocol: 'Active Sham' cases were identified only at the end of the experiment (transducer dislocation discovered by visual/MRI inspection), so 'the experimenters were blind to the experimental conditions for Active Sham or TUS groups during the experiment.' Coded as single-blind.
  • sham_typeThe sham/control group combined three distinct mechanisms: one animal given deliberately zero TUS intensity (inactive_transducer), three animals where the transducer was unintentionally off-target due to movement (not a designed sham, coded as other), plus a within-subject active non-LGN control-site sonication used in the LGN-TUS group itself (active_control_site).
  • auditory_controlNo masking sound or deafening was used; auditory/electromagnetic confounds were instead addressed analytically via interleaved light-only vs light-plus-TUS vs TUS-only trials and a separate tofu-phantom EEG-artifact control experiment.
  • n_sessions_per_subjectMost animals underwent the protocol once, but one LGN-TUS animal and one Active-Sham animal each underwent the full procedure twice (12 and 3 days apart respectively); recorded as [1,2] rather than a single number.
  • exposures[0].in_situ.pressure_kpaIn-situ intensity/pressure were estimated retrospectively from ex vivo hydrophone measurements of transmission through each animal's excised skull cap, then combined with per-animal power settings; reported as a range across the 6 LGN experiments with means given in the quote.