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Transcranial focused ultrasound of the amygdala modulates fear network activation and connectivity

Tina Chou, Thilo Deckersbach, Bastien Guerin, Karianne Sretavan Wong, Benjamin M. Borron, Anish Kanabar, Ashley N. Hayden, Marina P. Long, Mohammad Daneshzand, Edward F. Pace-Schott, Darin D. Dougherty

Brain Stimulation 2024, 17, 312-320 · 10.1016/j.brs.2024.03.004

human healthyhealthyfmriautonomic physiologybehaviour

Abstract

Background Current noninvasive brain stimulation methods are incapable of directly modulating subcortical brain regions critically involved in psychiatric disorders. Transcranial Focused Ultrasound (tFUS) is a newer form of noninvasive stimulation that could modulate the amygdala, a subcortical region implicated in fear. Objective We investigated the effects of active and sham tFUS of the amygdala on fear circuit activation, skin conductance responses (SCR), and self-reported anxiety during a fear-inducing task. We also investigated amygdala tFUS' effects on amygdala-fear circuit resting-state functional connectivity. Methods Thirty healthy individuals were randomized in this double-blinded study to active or sham tFUS of the left amygdala. We collected fMRI scans, SCR, and self-reported anxiety during a fear-inducing task (participants viewed red or green circles which indicated the risk of receiving an aversive stimulus), as well as resting-state scans, before and after tFUS. Results Compared to sham tFUS, active tFUS was associated with decreased (pre to post tFUS) blood-oxygen-level-dependent fMRI activation in the amygdala (F(1,25) = 4.86, p = 0.04, η 2 = 0.16) during the fear task, and lower hippocampal (F(1,27) = 4.41, p = 0.05, η 2 = 0.14), and dorsal anterior cingulate cortex (F(1,27) = 6.26, p = 0.02; η 2 = 0.19) activation during the post tFUS fear task. The decrease in amygdala activation was correlated with decreased subjective anxiety (r = 0.62, p = 0.03). There was no group effect in SCR changes from pre to post tFUS (F(1,23) = 0.85, p = 0.37). The active tFUS group also showed decreased amygdala-insula (F(1,28) = 4.98, p = 0.03) and amygdala-hippocampal (F(1,28) = 7.14, p = 0.01) rsFC, and increased amygdala-ventromedial prefrontal cortex (F(1,28) = 3.52, p = 0.05) resting-state functional connectivity. Conclusions tFUS can change functional connectivity and brain region activation associated with decreased anxiety. Future studies should investigate tFUS' therapeutic potential for individuals with clinical levels of anxiety.

Abstract via europepmc.

Specieshuman
Subjects15 participants
Sessions per subject1
Randomisedyes
Blindingdouble
Sham / controlinactive transducer
Auditory controlnot reported
Readout timingoffline
Anaesthesianot applicable
Readoutsfmri, autonomic physiology, behaviourSkin conductance response (SCR); self-reported anxiety ratings (0-100 scale) during fear task; resting-state functional connectivity (CONN toolbox) with a left amygdala seed.
Direction of effectinhibitoryActive tFUS decreased amygdala, hippocampal, and dorsal anterior cingulate cortex BOLD activation during a fear task relative to sham; decreased amygdala-insula and amygdala-hippocampal resting-state connectivity and increased amygdala-vmPFC connectivity; the decrease in amygdala activation correlated with decreased self-reported anxiety (r=0.62).
Adverse eventsnone observedNo adverse effects were associated with active tFUS; two participants reported non-unpleasant vibration/tapping sensations at the transducer site during sonication that resolved after sonication ended.

Exposures

Exposure 1: active tFUS of left amygdala

Target: amygdala — “left amygdala
Device: BrainSonix · BrainSonix Corporation · BX Pulsar 1002

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)650✓✓
Pulse duration (ms)5✓✓
Pulse repetition frequency (Hz)10✓✓
Duty cycle (%)5pulse duration × PRF gives 5%✓✓
Sonication duration (s)30✓✓
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)not reported
In-situ Isppa (W/cm²)14.4✓✓
In-situ Ispta (W/cm²)0.72✓✓
Protocol, in the paper’s words

In the MRI scanner, the active tFUS group received 20 min total of 30-s on and 30-s off blocks of sonication to the left amygdala; a specific amygdala sub-nucleus was not targeted.

Flags from extraction

  • n_subjectsTotal enrolled was 30 (15 sham, 15 active); n_subjects reflects only the 15 participants who received active (real) tFUS, per the definition of 'subjects exposed to ultrasound'.
  • n_sessions_per_subjectThe paper describes a single scanning visit with pre/post tFUS measurements but never explicitly states the number of sessions per participant.