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Ultrasound Stimulations Induce Prolonged Depolarization and Fast Action Potentials in Leech Neurons

Francesca Dedola, Francesco Paolo Ulloa Severino, Nicolo Meneghetti, Theo Lemaire, Andrea Cafarelli, Leonardo Ricotti, Arianna Menciassi, Annarita Cutrone, Alberto Mazzoni, Silvestro Micera

IEEE Open Journal of Engineering in Medicine and Biology 2020 · 10.1109/ojemb.2019.2963474

invertebratehealthyinvasive electrophysiology

Abstract

Objective: Ultrasound (US) stimulation carries the promise of a selective, reversible, and non-invasive modulation of neural activity without the need for genetic manipulation of neural structures. However, the mechanisms of US-induced generation of action potentials (APs) are still unclear. Methods: Here we address this issue by analyzing intracellularly recorded responses of leech nociceptive neurons to controlled delivery of US. Results: US induced a depolarization linearly accumulating in time and outlasting the duration of the stimulation. Spiking activity was reliably induced for an optimal US intensity range. Moreover, we found that APs induced by US differ in smaller amplitude and faster repolarization from those induced by electrical stimulation in the same cell but display the same repolarization rate. Conclusions: These results shed light on the mechanism by which spikes are induced by US and pave the way for designing more efficient US stimulation patterns.

Abstract via europepmc.

Speciesmedicinal leech (Hirudo medicinalis)
Subjects47, 23swept preparations
Sessions per subjectnot applicable
Randomisednot reported
Blindingnot reported
Sham / controlnone
Auditory controlnot reported
Readout timingboth
Anaesthesianot reported
Readoutsinvasive electrophysiologyintracellular sharp-electrode recording of membrane potential (Ag/AgCl electrode)
Direction of effectexcitatoryUS induced a depolarization that accumulated linearly in time, outlasted the stimulus, and reliably triggered action potentials in N cells (27/44 recorded cells) over an optimal intensity range, with depolarization and spike probability increasing with both pressure and duty cycle (summarized by Ispta); P cells showed much smaller depolarization and rarely spiked.
Adverse eventsnot reported

Exposures

Exposure 1: Leech ganglion nociceptive (N) and pressure (P) mechanosensory neurons

Target: leech neurons — “leech ganglion nociceptive (N) and pressure (P) mechanosensory neurons
Device: other named manufacturer · Precision Acoustics LTD

Pulse timing
Waveformpulsed, continuous
Fundamental frequency (kHz)490✓✓
Pulse duration (ms)5, 50, 100swept✓✓
Pulse repetition frequency (Hz)10✓✓
Duty cycle (%)5, 50, 100swept✓✓
Sonication duration (s)0.3✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)8, 12, 16, 20swept✓✓
Free-field Isppa (W/cm²)not reported
Free-field Ispta (W/cm²)0.0002, 0.027swept✓✓
In-situ estimatenot applicable
In-situ pressure (kPa)not applicable
In-situ Isppa (W/cm²)not applicable
In-situ Ispta (W/cm²)not applicable
Protocol, in the paper’s words

Sinusoidal tone bursts at 490 kHz were delivered at a pulse repetition frequency of 10 Hz (pulse repetition period 100 ms) for a total stimulus duration of 300 ms per stimulation window; duty cycle was fixed at 5%, 50% or 100% (T-on of 5, 50 or 100 ms respectively within the 100-ms period; 100% DC is continuous, i.e. no off-time). Each 300-ms stimulation was repeated 3 times during a recording session with an inter-stimulation interval of 20-30 s; electrical pulses were used to generate a single spike in N cells before and after each US window to confirm cell health.

Flags from extraction

  • exposures[0].free_field.pressure_kpathe Methods section (Ultrasound Calibration) states the transducer was 'characterized in free field conditions', but the Results text separately states the root-mean-square pressure was 'evaluated in the Petri dish containing the pinned ganglia'; domain is therefore somewhat ambiguous between free-field water-tank calibration and an at-target (in-dish) measurement, recorded here as free_field per the explicit 'free field conditions' statement.
  • exposures[0].timing.duty_cycle_pctduty cycle of 100% corresponds to continuous-wave stimulation (T-on = full 100-ms period, no off-time); merged into a single exposure with the pulsed 5% and 50% duty-cycle conditions as a parameter sweep at the same target and frequency.
  • n_subjects47 N cells and 23 P cells were both stimulated with ultrasound (70 total); the paper does not separately break down how many leeches these cells came from.
  • anaesthesialeeches were kept at 5C and dissected in chilled Ringer's solution, but the paper does not explicitly describe this as anaesthesia; the isolated ganglion preparation itself was not anaesthetised during ultrasound delivery.