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Dynamic changes in human brain connectivity following ultrasound neuromodulation

Cyril Atkinson-Clement, Mohammad Alkhawashki, Marilyn Gatica, James Ross, Marcus Kaiser

Scientific Reports 2024, 14 · 10.1038/s41598-024-81102-w

human healthyhealthyfmribehaviour

Abstract

Non-invasive neuromodulation represents a major opportunity for brain interventions, and transcranial focused ultrasound (FUS) is one of the most promising approaches. However, some challenges prevent the community from fully understanding its outcomes. We aimed to address one of them and unravel the temporal dynamics of FUS effects in humans. Twenty-two healthy volunteers participated in the study. Eleven received FUS in the right inferior frontal cortex while the other 11 were stimulated in the right thalamus. Using a temporal dynamic approach, we compared resting-state fMRI seed-based functional connectivity obtained before and after FUS. We also assessed behavioural changes as measured with a task of reactive motor inhibition. Our findings reveal that the effects of FUS are predominantly time-constrained and spatially distributed in brain regions functionally connected with the directly stimulated area. In addition, mediation analysis highlighted that FUS applied in the right inferior cortex was associated with behavioural alterations which was directly explained by the applied acoustic pressure and the brain functional connectivity change we observed. Our study underscored that the biological effects of FUS are indicative of behavioural changes observed more than an hour following stimulation and are directly related to the applied acoustic pressure.

Abstract via europepmc.

Specieshuman
Subjects22 participants
Sessions per subject1
Randomisedyes
Blindingnone
Sham / controlnone
Auditory controlnot reported
Readout timingoffline
Anaesthesianot applicable
Readoutsfmri, behaviourResting-state fMRI seed-based functional connectivity (right IFC or right thalamus seed); stop-signal task (Go-trial reaction time, stop-signal reaction time)
Direction of effectmixed or unclearIFC-FUS decreased functional connectivity between right IFC and six regions (post-central cortex, ACC, SFC, MTC, OFC, lingual cortex) and decreased Go-trial reaction time, an effect correlated with the applied peak pressure and with IFC-post-central disconnection; stop-signal reaction time was unchanged. Thalamus-FUS decreased connectivity with left SMA and right MFC but increased connectivity with contralateral cerebellum and thalamus, with no behavioural change.
Adverse eventsobservedThree participants reported transient side effects within one hour of FUS (dizziness, muscle spasms in the right eye corner, and lack of coordination; small muscle twitches in the legs; confusion by MRI scanner sound); none were reported thereafter.

Exposures

Exposure 1: Right inferior frontal cortex (IFC) theta-burst FUS

Target: inferior frontal gyrus — “right inferior frontal cortex (IFC)
Device: NeuroFUS · Sonic Concepts (sold by Brainbox) · NeuroFUS PRO TPO-203 with CTX-500-4CH transducer

Pulse timing
Waveformtheta burst
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)20✓✓
Pulse repetition frequency (Hz)5✓✓
Duty cycle (%)10pulse duration × PRF gives 10%✓✓
Sonication duration (s)80✓✓
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 estimatesimulationmean or range across subjects
In-situ pressure (kPa)153.5✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)0.0833✓✓
Isppa, domain unspecified (W/cm²)54.51✓✓
Protocol, in the paper’s words

Individualised acoustic simulations (using each participant's ZTE-derived skull map) were used to select the transducer trajectory minimising skull thickness to the target; the theta-burst FUS protocol was delivered once, immediately followed by an MRI session (~15 min delay) and a cognitive task (~70 min delay).

Exposure 2: Right thalamus theta-burst FUS

Target: thalamus — “right thalamus (centroid of whole thalamus)
Device: NeuroFUS · Sonic Concepts (sold by Brainbox) · NeuroFUS PRO TPO-203 with CTX-500-4CH transducer

Pulse timing
Waveformtheta burst
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)20✓✓
Pulse repetition frequency (Hz)5✓✓
Duty cycle (%)10pulse duration × PRF gives 10%✓✓
Sonication duration (s)80✓✓
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 estimatesimulationmean or range across subjects
In-situ pressure (kPa)134.8✓✓
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)0.155✓✓
Isppa, domain unspecified (W/cm²)54.51✓✓
Protocol, in the paper’s words

Individualised acoustic simulations (using each participant's ZTE-derived skull map) were used to select the transducer trajectory minimising skull thickness to the target; the theta-burst FUS protocol was delivered once, immediately followed by an MRI session (~15 min delay) and a cognitive task (~70 min delay).

Flags from extraction

  • n_sessions_per_subjectInferred as one stimulation session (FUS given once, at the second visit); the paper does not state this as an explicit count.
  • exposures[0].timing.pulse_repetition_frequency_hzPRF was computed from the stated pulse repetition interval (200 ms -> 5 Hz), a period-to-frequency unit conversion rather than independent arithmetic.
  • exposures[0].unspecified_domain.isppa_w_cm2The device ISPPA setting (54.51 W/cm2) is not stated as free-field or in-situ; placed in unspecified_domain, while the per-target simulated pressure/ISPTA from Table 1 are placed in in_situ.
  • blindingPaper explicitly compares post- vs pre-FUS sessions 'without a proper placebo (i.e., sham stimulation)'; no blinding procedure is described.