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Low-intensity focused ultrasound to the insula differentially modulates the heartbeat-evoked potential: A proof-of-concept study

Andrew Strohman, Gabriel Isaac, Brighton Payne, Charles Verdonk, Sahib S. Khalsa, Wynn Legon

Clinical Neurophysiology 2024, 167, 267-281 · 10.1016/j.clinph.2024.09.006

human healthyhealthyeeg megautonomic physiology

Abstract

Objective The heartbeat evoked potential (HEP) is a brain response time-locked to the heartbeat and a potential marker of interoceptive processing that may be generated in the insula and dorsal anterior cingulate cortex (dACC). Low-intensity focused ultrasound (LIFU) can selectively modulate sub-regions of the insula and dACC to better understand their contributions to the HEP. Methods Healthy participants (n = 16) received stereotaxically targeted LIFU to the anterior insula (AI), posterior insula (PI), dACC, or Sham at rest during continuous electroencephalography (EEG) and electrocardiography (ECG) recording on separate days. Primary outcome was HEP amplitudes. Relationships between LIFU pressure and HEP changes and effects of LIFU on heart rate and heart rate variability (HRV) were also explored. Results Relative to sham, LIFU to the PI, but not AI or dACC, decreased HEP amplitudes; PI effects were partially explained by increased LIFU pressure. LIFU did not affect heart rate or HRV. Conclusions These results demonstrate the ability to modulate HEP amplitudes via non-invasive targeting of key interoceptive brain regions. Significance Our findings have implications for the causal role of these areas in bottom-up heart-brain communication that could guide future work investigating the HEP as a marker of interoceptive processing in healthy and clinical populations.

Abstract via europepmc.

Specieshuman
Subjects16 participants
Sessions per subject3
Randomisedyes
Blindingnot reported
Sham / controlinactive transducer
Auditory controlmasking sound
Readout timingonline
Anaesthesianot applicable
Readoutseeg meg, autonomic physiologyHeartbeat-evoked potential (HEP) amplitude at Cz; heart rate; heart rate variability (SDNN, HF power, LF power, LF/HF ratio)
Direction of effectmixed or unclearLIFU to the posterior insula (PI) decreased HEP amplitude relative to Sham (274-286 ms) and relative to dACC (648-661 ms), consistent with an inhibitory effect; LIFU to the anterior insula (AI) and dACC did not differ from Sham at either time window, though AI differed from dACC in the second window.
Adverse eventsobservedAfter adjustment, there were no new moderate or severe symptoms across any condition for all queried symptoms; the most common new symptom was mild sleepiness.

Exposures

Exposure 1: LIFU to anterior insula (AI)

Target: anterior insula — “anterior insula (AI, left dorsal anterior short gyrus)
Device: Sonic Concepts · Sonic Concepts · H-281

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)not reportedimplied by duty cycle ÷ PRF: 0.36 ms (not stated by the paper)
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)36✓✓
Sonication duration (s)1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)380✓✓
Free-field Isppa (W/cm²)4.2✓✓
Free-field Ispta (W/cm²)1.51✓✓
In-situ estimatesimulationmean or range across subjects
In-situ pressure (kPa)179.8✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

100 stimulations (1 s burst duration each) delivered with a fixed inter-stimulus interval of 5 s for a total application time of 10 min, with continuous auditory masking throughout.

Exposure 2: LIFU to posterior insula (PI)

Target: posterior insula — “posterior insula (PI, left dorsal posterior long gyrus)
Device: Sonic Concepts · Sonic Concepts · H-281

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)not reportedimplied by duty cycle ÷ PRF: 0.36 ms (not stated by the paper)
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)36✓✓
Sonication duration (s)1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)380✓✓
Free-field Isppa (W/cm²)4.2✓✓
Free-field Ispta (W/cm²)1.51✓✓
In-situ estimatesimulationmean or range across subjects
In-situ pressure (kPa)262.8✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

100 stimulations (1 s burst duration each) delivered with a fixed inter-stimulus interval of 5 s for a total application time of 10 min, with continuous auditory masking throughout.

Exposure 3: LIFU to dorsal anterior cingulate cortex (dACC)

Target: dorsal anterior cingulate cortex — “dorsal anterior cingulate cortex (dACC, MNI [0,18,30])
Device: Sonic Concepts · Sonic Concepts · H-104

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)not reportedimplied by duty cycle ÷ PRF: 0.36 ms (not stated by the paper)
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)36✓✓
Sonication duration (s)1✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)400✓✓
Free-field Isppa (W/cm²)4.5✓✓
Free-field Ispta (W/cm²)1.62✓✓
In-situ estimatesimulationmean or range across subjects
In-situ pressure (kPa)115.1✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

100 stimulations (1 s burst duration each) delivered with a fixed inter-stimulus interval of 5 s for a total application time of 10 min, with continuous auditory masking throughout.

Flags from extraction

  • exposures[0].in_situ.isppa_w_cm2Only in-situ pressure (derated) is reported per subject/target; derated intensity values are not given.
  • direction_of_effectEffects differ by target (PI inhibitory vs Sham/dACC; AI/dACC no effect vs Sham) so a single top-level direction is an approximation; see direction_notes.