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Transcranial focused ultrasound pulsation suppresses pentylenetetrazol induced epilepsy in vivo

Sin-Guang Chen, Chih-Hung Tsai, Chia-Jung Lin, Cheng-Chia Lee, Hsiang-Yu Yu, Tsung-Hsun Hsieh, Hao-Li Liu

Brain Stimulation 2020, 13, 35-46 · 10.1016/j.brs.2019.09.011

rodentepilepsyeeg megbehaviourhistology molecular

Abstract

Background Epilepsy is a neurological disorder characterized by abnormal neuron discharge, and one-third of epilepsy patients suffer from drug-resistant epilepsy (DRE). The current management for DRE includes epileptogenic lesion resection, disconnection, and neuromodulation. Neuromodulation is achieved through invasive electrical stimulus including deep brain stimulation, vagus nerve stimulation, or responsive neurostimulation (RNS). As an alternative therapy, transcranial focused ultrasound (FUS) can transcranially and non-invasively modulate neuron activity. Objective This study seeks to verify the use of FUS pulsations to suppress spikes in an acute epileptic small-animal model, and to investigate possible biological mechanisms by which FUS pulsations interfere with epileptic neuronal activity. Methods The study used a total of 76 Sprague-Dawley rats. For the epilepsy model, rats were administered pentylenetetrazol (PTZ) to induce acute epileptic-like abnormal neuron discharges, followed by FUS exposure. Various ultrasound parameters were set to test the epilepsy-suppressing effect, while concurrently monitoring and analyzing electroencephalogram (EEG) signals. Animal behavior was monitored and histological examinations were conducted to evaluate the hazard posed by ultrasound exposure and the expression of neuronal activity markers. Western blotting was used to evaluate the correlation between FUS-induced epileptic suppression and the PI3K-mTOR signaling pathway. Results We observed that FUS pulsations effectively suppressed epileptic activity and observed EEG spectrum oscillations; the spike-suppressing effect depended on the selection of ultrasound parameters and highly correlated with FUS exposure level. Expression level changes of c-Fos and GAD65 were confirmed in the cortex and hippocampus, indicating that FUS pulsations deactivated excitatory cells and activated GABAergic terminals. No tissue damage, inflammatory response, or behavioral abnormalities were observed in rats treated with FUS under these exposure parameters. We also found that the FUS pulsations down-regulated the S6 phosphorylation and decreased pAKT expression. Conclusion Our results suggest that pulsed FUS exposure effectively suppresses epileptic spikes in an acute epilepsy animal model, and finds that ultrasound pulsation interferes with neuronal activity and affects the PTZ-induced PI3K-Akt-mTOR pathway, which might help explain the mechanism underlying ultrasound-related epileptic spike control.

Abstract via europepmc.

Speciesrat (Sprague-Dawley)
Subjects6, 15, 6, 7, 22swept animals
Sessions per subjectnot reported
Randomisednot reported
Blindingsingle
Sham / controlundescribed
Auditory controlnot reported
Readout timingboth
Anaesthesiaanaesthetised
Readoutseeg meg, behaviour, histology molecularEEG spike/burst counting and power spectral density analysis; rotarod motor performance; c-Fos, GAD65, GFAP immunohistochemistry; H&E staining; western blot (phospho-S6, phospho-Akt)
Direction of effectinhibitoryFUS pulsation reduced PTZ-induced epileptic EEG spike/burst counts and power spectral density (including gamma band), increased GAD65 (inhibitory synapse marker) and decreased c-Fos (activation marker) in cortex, and attenuated PTZ-induced phospho-S6 and phospho-Akt; the suppressive effect scaled with acoustic pressure level (MI) and exposure time.
Adverse eventsnone observedNo obvious adverse reaction was observed in rats treated with acoustic level 6 exposure over 24 h; H&E and GFAP staining showed no tissue disruption, immune cell infiltration, microglia activation or astrogliosis, and no significant difference in rotarod performance or body weight was found in FUS-treated rats.

Exposures

Exposure 1: FUS parametric sweep (acoustic levels 1-5) along cortex-hippocampus-thalamus trajectory in PTZ-induced epilepsy

Target: cerebral cortex, hippocampus, thalamus — “cortex, hippocampus and thalamus (FUS beam trajectory)
Device: Sonic Concepts · SonicConcept

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)not reported
Pulse repetition frequency (Hz)100✓✓
Duty cycle (%)8, 30swept✓✓
Sonication duration (s)100, 600swept✓✓
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)0, 530swept✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)0.703, 0.75, 1.25, 2.81swept✓✓
Protocol, in the paper’s words

Six acoustic exposure levels (Table 1) combined MI 0-0.75, duty cycle 8% or 30%, and total exposure time 100 or 600 s at a fixed PRF of 100 Hz; level 0 (PTZ only, no FUS) served as control. FUS was delivered during a 30-min EEG recording session following intraperitoneal PTZ injection (100 mg/kg); a separate cohort received 3 repeated FUS sessions (days 0, 2, 4) for rotarod/behavioural safety testing.

Flags from extraction

  • n_subjects56 is the sum of animals in FUS-exposed acoustic levels 1-5 from Table 1 (excluding the 20 acoustic-level-0 PTZ-only controls); the paper does not give this total directly as one number.
  • exposures[0].unspecified_domain.pressure_kpaThe paper's own phrase 'free-field measured pressure level after considering 10% transcranial pressure loss' mixes free-field and transcranially-corrected wording, so the domain (free_field vs in_situ) is ambiguous; placed in unspecified_domain.
  • exposures[0].target.termsThe paper describes the FUS beam trajectory as passing through cortex, hippocampus and thalamus rather than naming one specific focal target nucleus.
  • sham_typeThe acoustic-level-0 PTZ-only control group's ultrasound-apparatus procedure (if any, e.g. mock positioning) is not described.
  • n_sessions_per_subjectThe EEG/spike-suppression cohort received a single FUS session, while a separate cohort for rotarod safety testing received FUS on days 0, 2 and 4 (3 sessions); no single per-subject count applies to the whole study.