← Explore

A frontopolar-temporal circuit determines the impact of social information in macaque decision making

Ali Mahmoodi, Caroline Harbison, Alessandro Bongioanni, Andrew Emberton, Lea Roumazeilles, Jerome Sallet, Nima Khalighinejad, Matthew F.S. Rushworth

Neuron 2024, 112, 84-92.e6 · 10.1016/j.neuron.2023.09.035

nonhuman primatehealthyfmribehaviour

Abstract

When choosing, primates are guided not only by personal experience of objects but also by social information such as others' attitudes toward the objects. Crucially, both sources of information-personal and socially derived-vary in reliability. To choose optimally, one must sometimes override choice guidance by personal experience and follow social cues instead, and sometimes one must do the opposite. The dorsomedial frontopolar cortex (dmFPC) tracks reliability of social information and determines whether it will be attended to guide behavior. To do this, dmFPC activity enters specific patterns of interaction with a region in the mid-superior temporal sulcus (mSTS). Reversible disruption of dmFPC activity with transcranial ultrasound stimulation (TUS) led macaques to fail to be guided by social information when it was reliable but to be more likely to use it when it was unreliable. By contrast, mSTS disruption uniformly downregulated the impact of social information on behavior.

Abstract via europepmc.

Speciesrhesus macaque (Macaca mulatta)
Subjects3 animals
Sessions per subject16
Randomisedyes
Blindingnot reported
Sham / controlinactive transducer
Auditory controlnot reported
Readout timingoffline
Anaesthesiaboth
Readoutsfmri, behaviourBinary choice accuracy in face/object social-information task; whole-brain fMRI GLM analyses of face-direction encoding (Experiment 1) and reliability-weighting (Experiment 2)
Direction of effectbidirectionaldmFPC-TUS reduced accuracy (relative to sham) both in incongruent face trials, where animals failed to follow reliable social information, and in incongruent object trials, where animals became more likely to be swayed by unreliable social information; mSTS-TUS uniformly reduced reliance on face information regardless of reliability.
Adverse eventsnot reported

Exposures

Exposure 1: Frontal polar cortex (FPC/dmFPC) TUS

Target: anterior prefrontal cortex — “frontal polar cortex (FPC) / dorsomedial frontopolar cortex (dmFPC)
Device: NeuroFUS · Sonic Concepts (sold by Brainbox) · NeuroFUS CTX-250

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)30✓✓
Pulse repetition frequency (Hz)not reported
Duty cycle (%)not reported
Sonication duration (s)40✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)60✓✓
Free-field Ispta (W/cm²)not reported
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

The stimulation comprised 30ms bursts of ultrasound, for a total stimulation duration of 40s. All targets were sonicated bilaterally for 80 s in total, with 40 s of stimulation applied to a target in each hemisphere (except for FPC which was only stimulated for 40s as the target was on the midline).

Exposure 2: Medial superior temporal sulcus (mSTS) TUS

Target: superior temporal gyrus — “medial superior temporal sulcus (mSTS)
Device: NeuroFUS · Sonic Concepts (sold by Brainbox) · NeuroFUS CTX-250

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)30✓✓
Pulse repetition frequency (Hz)not reported
Duty cycle (%)not reported
Sonication duration (s)40✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)60✓✓
Free-field Ispta (W/cm²)not reported
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

The stimulation comprised 30ms bursts of ultrasound, for a total stimulation duration of 40s. All targets were sonicated bilaterally for 80 s in total, with 40 s of stimulation applied to a target in each hemisphere. Sonication of the target in one hemisphere was immediately followed by sonication of a homologous target in the contralateral hemisphere.

Exposure 3: Extrastriate visual cortex (EVC) TUS

Target: extrastriate visual cortex — “extrastriate visual cortex (EVC)
Device: NeuroFUS · Sonic Concepts (sold by Brainbox) · NeuroFUS CTX-250

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)30✓✓
Pulse repetition frequency (Hz)not reported
Duty cycle (%)not reported
Sonication duration (s)40✓✓
Pressure and intensity, by domain
Free-field pressure (kPa)not reported
Free-field Isppa (W/cm²)60✓✓
Free-field Ispta (W/cm²)not reported
In-situ estimatenot reported
In-situ pressure (kPa)not reported
In-situ Isppa (W/cm²)not reported
In-situ Ispta (W/cm²)not reported
Protocol, in the paper’s words

The stimulation comprised 30ms bursts of ultrasound, for a total stimulation duration of 40s. All targets were sonicated bilaterally for 80 s in total, with 40 s of stimulation applied to a target in each hemisphere. Note that the precise EVC coordinate reported in the fMRI results was not accessible to the TUS coil, so a nearby accessible coordinate associated with qualitatively identical activity patterns was used instead.

Flags from extraction

  • exposures[0].timing.pulse_repetition_frequency_hzPaper states 30 ms ultrasound bursts totaling 40 s of stimulation but never states the pulse repetition frequency or duty cycle needed to reconcile burst duration with total duration.
  • direction_of_effectEffect direction depends on trial type (face vs object, congruent vs incongruent); classified as bidirectional rather than simple excitatory/inhibitory.
  • anaesthesiaAnimals were awake for behavioral/TUS sessions but anesthetized for the separate structural MRI scan.