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Transcranial focused ultrasound selectively increases perfusion and modulates functional connectivity of deep brain regions in humans

Taylor Kuhn, Norman M. Spivak, Bianca H. Dang, Sergio Becerra, Sabrina E. Halavi, Natalie Rotstein, Benjamin M. Rosenberg, Sonja Hiller, Andrew Swenson, Luka Cvijanovic, Nolan Dang, Michael Sun, David Kronemyer, Rustin Berlow, Malina R. Revett, Nanthia Suthana, Martin M. Monti, Susan Bookheimer

Frontiers in Neural Circuits 2023, 17 · 10.3389/fncir.2023.1120410

human healthyhealthyfmriother mri

Abstract

Background Low intensity, transcranial focused ultrasound (tFUS) is a re-emerging brain stimulation technique with the unique capability of reaching deep brain structures non-invasively. Objective/hypothesis We sought to demonstrate that tFUS can selectively and accurately target and modulate deep brain structures in humans important for emotional functioning as well as learning and memory. We hypothesized that tFUS would result in significant longitudinal changes in perfusion in the targeted brain region as well as selective modulation of BOLD activity and BOLD-based functional connectivity of the target region. Methods In this study, we collected MRI before, simultaneously during, and after tFUS of two deep brain structures on different days in sixteen healthy adults each serving as their own control. Using longitudinal arterial spin labeling (ASL) MRI and simultaneous blood oxygen level dependent (BOLD) functional MRI, we found changes in cerebral perfusion, regional brain activity and functional connectivity specific to the targeted regions of the amygdala and entorhinal cortex (ErC). Results tFUS selectively increased perfusion in the targeted brain region and not in the contralateral homolog or either bilateral control region. Additionally, tFUS directly affected BOLD activity in a target specific fashion without engaging auditory cortex in any analysis. Finally, tFUS resulted in selective modulation of the targeted functional network connectivity. Conclusion We demonstrate that tFUS can selectively modulate perfusion, neural activity and connectivity in deep brain structures and connected networks. Lack of auditory cortex findings suggests that the mechanism of tFUS action is not due to auditory or acoustic startle response but rather a direct neuromodulatory process. Our findings suggest that tFUS has the potential for future application as a novel therapy in a wide range of neurological and psychiatric disorders associated with subcortical pathology.

Abstract via europepmc.

Specieshuman
Subjects18 participants
Sessions per subject2
Randomisedyes
Blindingdouble
Sham / controlnone
Auditory controlnot reported
Readout timingboth
Anaesthesianot applicable
Readoutsfmri, other mriArterial spin labeling (ASL) perfusion MRI; psychophysiological interaction (PPI) functional connectivity analysis
Direction of effectbidirectionalAmygdala tFUS (disruptive parameters) decreased BOLD activity and decreased functional connectivity between amygdala and its network; ErC tFUS (excitatory parameters) increased BOLD/connectivity in ErC network (though some regions showed reduced BOLD). Both increased regional perfusion in the targeted region.
Adverse eventsnone observedNo adverse events occurred during this study. Participants were followed every day for three days following each tFUS session and exhibited no negative reactions, including physical discomfort or heightened anxiety.

Exposures

Exposure 1: Amygdala tFUS (disruptive paradigm)

Target: amygdala — “right amygdala
Device: BrainSonix · BrainSonix Corp.

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)not reported
In-situ Ispta (W/cm²)0.72✓✓
Protocol, in the paper’s words

Both paradigms used a 5% duty cycle, in 10 cycles of 30 s on, 30 s off, for a total of 5 min of non-consecutive tFUS. The amygdala paradigm used a 5 ms pulse width at 10 Hz PRF, hypothesized to disrupt/inhibit amygdala activity.

Exposure 2: Entorhinal cortex (ErC) tFUS (excitatory paradigm)

Target: entorhinal cortex — “left entorhinal cortex (ErC)
Device: BrainSonix · BrainSonix Corp.

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)650✓✓
Pulse duration (ms)0.5✓✓
Pulse repetition frequency (Hz)100✓✓
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)not reported
In-situ Ispta (W/cm²)0.72✓✓
Protocol, in the paper’s words

Both paradigms used a 5% duty cycle, in 10 cycles of 30 s on, 30 s off, for a total of 5 min of non-consecutive tFUS. The ErC paradigm used a 0.5 ms pulse width at 100 Hz PRF, hypothesized to increase/excite ErC activity.

Flags from extraction

  • exposures[0].device.modelDevice is attributed to BrainSonix Corp but no specific model number is given in the main text.
  • exposures[0].timing.sonication_duration_sRecorded as the 30-s active block length; the paper separately reports a total of 5 min of non-consecutive tFUS across 10 such blocks (see protocol_description).
  • n_sessions_per_subjectInferred as 2 from the two-session crossover design (one per target); not stated as a bare number.