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Displacement Imaging for Focused Ultrasound Peripheral Nerve Neuromodulation

Stephen A. Lee, Hermes A. S. Kamimura, Mark T. Burgess, Elisa E. Konofagou

IEEE Transactions on Medical Imaging 2020, 39, 3391-3402 · 10.1109/tmi.2020.2992498

rodenthealthyemg mephistology molecularbehaviourother

Abstract

Focused ultrasound (FUS) is an emerging technique for neuromodulation due to its noninvasive application and high depth penetration. Recent studies have reported success in modulation of brain circuits, peripheral nerves, ion channels, and organ structures. In particular, neuromodulation of peripheral nerves and the underlying mechanisms remain comparatively unexplored in vivo. Lack of methodologies for FUS targeting and monitoring impede further research in in vivo studies. Thus, we developed a method that non-invasively measures nerve engagement, via tissue displacement, during FUS neuromodulation of in vivo nerves using simultaneous high frame-rate ultrasound imaging. Using this system, we can validate, in real-time, FUS targeting of the nerve and characterize subsequent compound muscle action potentials (CMAPs) elicited from sciatic nerve activation in mice using 0.5 to 5 ms pulse durations and 22 - 28 MPa peak positive stimulus pressures at 4 MHz. Interestingly, successful motor excitation from FUS neuromodulation required a minimum interframe nerve displacement of 18 μm without any displacement incurred at the skin or muscle levels. Moreover, CMAPs detected in mice monotonically increased with interframe nerve displacements within the range of 18 to 300 μm . Thus, correlation between nerve displacement and motor activation constitutes strong evidence FUS neuromodulation is driven by a mechanical effect given that tissue deflection is a result of highly focused acoustic radiation force.

Abstract via europepmc.

Speciesmouse (C57BL/6J)
Subjects6, 5swept animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlundescribed
Auditory controlnot reported
Readout timingboth
Anaesthesiaanaesthetised
Readoutsemg mep, histology molecular, behaviour, othercompound muscle action potentials (CMAP) via EMG; high frame-rate ultrasound displacement/elastography imaging of the nerve; passive cavitation mapping; H&E histology; CatWalk gait analysis (sciatic function index, paw print)
Direction of effectexcitatoryHigher-pressure, and to a lesser extent longer-duration, FUS pulses produced larger CMAP amplitudes and higher probability of motor activation (excitation) of the sciatic nerve, correlated with greater acoustic-radiation-force-induced nerve displacement.
Adverse eventsnone observedH&E stains show that sonications at all parameters explored in the study appear safe and do not show apparent damage compared to sham sonications. There is no red blood cell extravasation or myelin disruption characteristic of damage to the sciatic nerve.

Exposures

Exposure 1: Sciatic nerve FUS parameter sweep (pressure and pulse duration)

Target: sciatic nerve — “sciatic nerve
Device: Sonic Concepts · Sonic Concepts Inc. · H-215

Pulse timing
Waveformcontinuous
Fundamental frequency (kHz)4,000✓✓
Pulse duration (ms)not applicable
Pulse repetition frequency (Hz)not applicable
Duty cycle (%)100?
Sonication duration (s)0.0005, 0.01swept✓✓
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 estimatederatingsingle value
In-situ pressure (kPa)4,000, 30,000swept✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

The acoustic pressure was varied from 4 to 30 MPa in steps of 4 MPa and the pulse duration was varied from 0.5 to 10 ms in steps of 0.5 ms; single pulses were emitted at 0.03 Hz to mitigate cumulative bioeffects. A base parameter of 24 MPa and 1 ms was used for follow-up displacement/safety experiments. A separate histology safety experiment applied 100 pulses (22-30 MPa, 1 ms) at a stated PRF of 0.2 Hz in the Methods text but 0.3 Hz in the corresponding figure caption. Gait-analysis safety experiments used 10 sonications (24 MPa, 1 ms, 30 s inter-stimulus interval).

Flags from extraction

  • n_subjectsPaper reports separate animal counts for different sub-experiments (parameter-space mapping n=6; focal-depth displacement experiment n=4; histology safety n=6 nerves; gait analysis n=10, 5 sham/5 FUS) without a single combined total; a preliminary cavitation-mapping follow-up (147 sonications) does not state a distinct animal count and is not included in the list.
  • sham_typeSham sonications are mentioned (e.g., 'sham ultrasound', '5 sham' mice) but the paper never describes how the sham was delivered (transducer off, blocked, etc.).
  • exposures[0].free_field.pressure_kpa6.5 MPa is a hydrophone beam-characterization value measured in free field water for FWHM mapping, distinct from the muscle-derated pressures (4-30 MPa) used to dose the sciatic nerve; both are reported here in their respective domains.
  • exposures[0].in_situ.pressure_kpaAppendix A states that 'All pressures reported in this study are derated for attenuation in muscle tissue', so the 4-30 MPa sweep values used throughout Methods/Results are treated as in_situ (muscle-derated), not free-field, values.
  • exposures[0].timing.protocol_descriptionText (Methods, section J) states the histology PRF was 0.2 Hz while the Figure 8 caption states 0.3 Hz for the same experiment; this text-vs-figure disagreement could not be resolved.
  • exposures[0].timing.pulse_duration_msIndividual ms-scale bursts (0.5-10 ms) have no internal pulsing and are repeated at a very low external rate (0.03-0.3 Hz); classified as waveform=continuous per the schema's tone-burst rule, with the burst length recorded as sonication_duration_s rather than pulse_duration_ms.