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Transcranial focused ultrasound to human rIFG improves response inhibition through modulation of the P300 onset latency

Justin M Fine, Archana S Mysore, Maria E Fini, William J Tyler, Marco Santello

eLife 2023, 12 · 10.7554/elife.86190

human healthyhealthyeeg megbehaviour

Abstract

Response inhibition in humans is important to avoid undesirable behavioral action consequences. Neuroimaging and lesion studies point to a locus of inhibitory control in the right inferior frontal gyrus (rIFG). Electrophysiology studies have implicated a downstream event-related potential from rIFG, the fronto-central P300, as a putative neural marker of the success and timing of inhibition over behavioral responses. However, it remains to be established whether rIFG effectively drives inhibition and which aspect of P300 activity uniquely indexes inhibitory control-ERP timing or amplitude. Here, we dissect the connection between rIFG and P300 for inhibition by using transcranial-focused ultrasound (tFUS) to target rIFG of human subjects while they performed a Stop-Signal task. By applying tFUS simultaneously with different task events, we found behavioral inhibition was improved, but only when applied to rIFG simultaneously with a 'stop' signal. Improved inhibition through tFUS to rIFG was indexed by faster stopping times that aligned with significantly shorter N200/P300 onset latencies. In contrast, P300 amplitude was modulated during tFUS across all groups without a paired change in behavior. Using tFUS, we provide evidence for a causal connection between anatomy, behavior, and electrophysiology underlying response inhibition.

Abstract via europepmc.

Specieshuman
Subjects25, 23swept participants
Sessions per subject1
Randomisedyes
Blindingnot reported
Sham / controlinactive transducer, active control site
Auditory controlsound only sham
Readout timingonline
Anaesthesianot applicable
Readoutseeg meg, behaviourStop-Signal Task (SSRT, P(respond|signal), Go reaction time); N200/P300 event-related potential amplitude and onset latency analysis
Direction of effectexcitatorytFUS to rIFG delivered simultaneously with the Stop signal improved response inhibition (lower probability of failing to inhibit, faster SSRT) and was associated with earlier N200/P300 onset latency that co-varied with the change in SSRT; no comparable behavioral or ERP-timing effects occurred for tFUS to rIFG timed with the Go signal, or for the S1 active-control or sham rIFG groups.
Adverse eventsnot reported

Exposures

Exposure 1: Online tFUS to right inferior frontal gyrus (rIFG, pars opercularis) during a Stop-Signal task

Target: inferior frontal gyrus — “right inferior frontal gyrus (rIFG), pars opercularis
Device: Blatek · Blatek

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)500✓✓
Pulse duration (ms)not reportedimplied by duty cycle ÷ PRF: 0.24 ms (not stated by the paper)
Pulse repetition frequency (Hz)1,000✓✓
Duty cycle (%)24✓✓
Sonication duration (s)0.5✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)820✓✓
Free-field Isppa (W/cm²)22.43✓✓
Free-field Ispta (W/cm²)5.38✓✓
In-situ estimatesimulationsingle value
In-situ pressure (kPa)540✓✓
In-situ Isppa (W/cm²)10.01✓✓
In-situ Ispta (W/cm²)2.4✓✓
Protocol, in the paper’s words

tFUS was delivered to rIFG for 500 ms, time-locked (t=0 ms) to either the Go signal or the Stop signal on a subset of Go and Stop trials, using a carrier frequency of 0.5 MHz, PRF of 1.0 kHz, and duty cycle of 24%. Each experimental session consisted of 1200 trials across 12 blocks of 100 trials, mixing stimulation and no-stimulation blocks; trial types were randomly distributed to mitigate carry-over effects.

Flags from extraction

  • n_subjectsThe Sham rIFG group (n=15) is excluded from n_subjects because the transducer was pointed away from the head and 'did not want substantial ultrasound energy transmitted'; only the rIFG (n=25) and S1 (n=23) groups received real tFUS to a cortical target, so both group sizes are listed.
  • exposures[0].timing.pulse_duration_msThe paper reports carrier frequency, PRF and duty cycle but never states the duration of the individual 0.5-MHz bursts triggered by channel 2; not computed from duty cycle/PRF per the no-arithmetic rule.