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Single cell RNA-sequencing reveals GINIP-expressing neurons as the main targets of focused ultrasound

Elena Brunet, Thibaud Parpaite, Sungjae Yoo, Eric Debieu, Khaled Metwally, Serge Mensah, Pascale Malapert, Andrew Saurin, Olivier Macherey, Emilie Franceschini, Aziz Moqrich

2024 · 10.1101/2024.07.17.604026

in vitro cellhealthycellular imaginghistology molecular

Abstract

Dorsal root ganglion (DRG) neurons have a wide range of functions, including touch, pain and itch. These neurons have emerged as promising targets for non-invasive focused ultrasound (FUS) neuromodulation. However, our knowledge of the molecular and physical mechanisms underlying FUS-evoked responses in DRG neurons is limited. Here, we investigate the neuromodulatory capabilities of FUS in cultured DRG neurons in combination with calcium imaging. We find that a 20-MHz FUS burst of 1-ms duration at an acoustic pressure of 5 MPa elicited calcium responses in 52% of DRG neurons. Single-cell RNA sequencing reveals that the majority of FUS-sensitive neurons belong to three subsets of DRG neurons; C-LTMRs, the MRGPRD-expressing C-HTMRs and A6-LTMRs. FUS excites all these neuronal subtypes by membrane deformation, suggesting a mechanism mediated by mechanosensitive ion channels. Our results identify FUS parameters that activate distinct subsets of DRG neurons and open new avenues for using FUS stimulation to modulate DRG neuron function.

Abstract via europepmc.

Speciesmouse
Subjects192 cultures
Sessions per subjectnot applicable
Randomisednot applicable
Blindingnot applicable
Sham / controlnone
Auditory controlnot reported
Readout timingboth
Anaesthesianot applicable
Readoutscellular imaging, histology molecularCalcium imaging (GCaMP6s / Fluo4-AM) of cultured DRG neurons; single-cell RNA sequencing; high-speed camera imaging of FUS-induced cell deformation.
Direction of effectexcitatoryFUS elicited calcium responses (activation) in cultured DRG neurons, increasing with acoustic pressure and stimulus duration; GINIP+ neurons (C-LTMRs, MRGPRD+ NP1) were preferentially activated.
Adverse eventsnot applicable

Exposures

Exposure 1: optimal FUS stimulus to cultured DRG neurons

Target: dorsal root ganglion culture — “cultured DRG neurons
Device: Olympus / Panametrics · Olympus · V317-SM

Pulse timing
Waveformcontinuous
Fundamental frequency (kHz)20,000✓✓
Pulse duration (ms)not applicable
Pulse repetition frequency (Hz)not applicable
Duty cycle (%)not applicable
Sonication duration (s)0.0001, 0.001swept?
Pressure and intensity, by domain
Free-field pressure (kPa)4,000, 5,000swept?
Free-field Isppa (W/cm²)346, 536swept?
Free-field Ispta (W/cm²)not reported
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

The FUS stimulus consisted of a 20-MHz sinusoidal signal with peak positive pressure of 4 to 5 MPa and stimulus duration of 0.1 to 1 ms. Each cell was subjected to a single FUS stimulus to avoid potential cumulative effects (the 'optimal FUS stimulus' was 5 MPa for 1 ms). For the scRNA-seq experiment, neurons instead received two consecutive optimal FUS stimulations 2 minutes apart; for the deformation experiments, neurons received up to 6-7 consecutive stimuli sweeping pressure or duration.

Flags from extraction

  • n_sessions_per_subjectMost cells received a single FUS stimulus (used for the pressure/duration dose-response and n=192 count), but the scRNA-seq and deformation sub-experiments used repeated stimulations (2 to 7 consecutive stimuli); n_sessions_per_subject=1 reflects the main dose-response experiment only.
  • exposures[0].free_field.pressure_kpaCells were in a dish/culture setup (no skull); paper describes the beam as 'free-field' (measured by hydrophone) so these values were placed in free_field, though this is a bath-type in vitro exposure rather than a whole-water free-field beam characterization for a transcranial study.
  • exposures[0].timing.pulse_duration_msClassified as continuous (single uninterrupted tone burst per trial) per the burst rule; sonication_duration_s carries the 0.1-1 ms burst length instead.