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General mechanisms of task engagement in the primate frontal cortex

Jan Grohn, Nima Khalighinejad, Caroline I Jahn, Alessandro Bongioanni, Urs Schüffelgen, Jerome Sallet, Matthew F. S. Rushworth, Nils Kolling

Nature Communications 2024, 15 · 10.1038/s41467-024-49128-w

nonhuman primatehealthybehaviour

Abstract

Staying engaged is necessary to maintain goal-directed behaviors. Despite this, engagement exhibits continuous, intrinsic fluctuations. Even in experimental settings, animals, unlike most humans, repeatedly and spontaneously move between periods of complete task engagement and disengagement. We, therefore, looked at behavior in male macaques (macaca mulatta) in four tasks while recording fMRI signals. We identified consistent autocorrelation in task disengagement. This made it possible to build models capturing task-independent engagement. We identified task general patterns of neural activity linked to impending sudden task disengagement in mid-cingulate gyrus. By contrast, activity centered in perigenual anterior cingulate cortex (pgACC) was associated with maintenance of performance across tasks. Importantly, we carefully controlled for task-specific factors such as the reward history and other motivational effects, such as response vigor, in our analyses. Moreover, we showed pgACC activity had a causal link to task engagement: transcranial ultrasound stimulation of pgACC changed task engagement patterns.

Abstract via europepmc.

Speciesrhesus macaque (Macaca mulatta)
Subjects4 animals
Sessions per subjectnot reported
Randomisednot reported
Blindingnot reported
Sham / controlundescribed
Auditory controlnot reported
Readout timingoffline
Anaesthesiaawake
ReadoutsbehaviourTime spent disengaged from a reward-based decision-making task, tracked across the testing session
Direction of effectmixed or unclearTUS of pgACC reduced disengagement (i.e., increased task engagement) specifically in the first 20 minutes of testing relative to BF, POp, and sham TUS; the underlying excitatory/inhibitory neural mechanism was not established and authors state TUS more likely disrupts endogenous activity than mimics excitation.
Adverse eventsnot reported

Exposures

Exposure 1: TUS of perigenual anterior cingulate cortex (pgACC)

Target: pregenual anterior cingulate cortex — “perigenual anterior cingulate cortex (pgACC)
Device: Sonic Concepts · Sonic Concept, Bothell, WA, USA · H115-MR

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)30✓✓
Pulse repetition frequency (Hz)10✓✓
Duty cycle (%)30pulse duration × PRF gives 30%✓✓
Sonication duration (s)40✓✓
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 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

TUS was applied in 30 ms bursts that were generated every 100 ms for a total period of 40 s. The procedure was then immediately repeated for another 40 s in the same area but in the other hemisphere. All TUS was applied prior to the behavioral task.

Exposure 2: TUS of basal forebrain (BF), control region

Target: basal forebrain — “basal forebrain (BF)
Device: Sonic Concepts · Sonic Concept, Bothell, WA, USA · H115-MR

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)30✓✓
Pulse repetition frequency (Hz)10✓✓
Duty cycle (%)30pulse duration × PRF gives 30%✓✓
Sonication duration (s)40✓✓
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 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

TUS was applied in 30 ms bursts that were generated every 100 ms for a total period of 40 s. The procedure was then immediately repeated for another 40 s in the same area but in the other hemisphere. All TUS was applied prior to the behavioral task.

Exposure 3: TUS of parietal operculum (POp), control region

Target: other — “parietal operculum (POp)
Device: Sonic Concepts · Sonic Concept, Bothell, WA, USA · H115-MR

Pulse timing
Waveformpulsed
Fundamental frequency (kHz)250✓✓
Pulse duration (ms)30✓✓
Pulse repetition frequency (Hz)10✓✓
Duty cycle (%)30pulse duration × PRF gives 30%✓✓
Sonication duration (s)40✓✓
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 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

TUS was applied in 30 ms bursts that were generated every 100 ms for a total period of 40 s. The procedure was then immediately repeated for another 40 s in the same area but in the other hemisphere. All TUS was applied prior to the behavioral task.

Flags from extraction

  • exposures[0].timing.pulse_repetition_frequency_hzPRF of 10 Hz derived from the stated repetition period (a burst every 100 ms); a unit conversion, not independent arithmetic.
  • sham_typePaper states a sham TUS condition was included but does not describe how the sham was implemented (e.g., inactive transducer vs other mechanism).
  • n_subjectsThe wider fMRI dataset includes 13 macaques, but only 4 macaques participated in the TUS sub-study; n_subjects here reflects only those exposed to ultrasound.
  • exposures[1].target.termsBasal forebrain (BF) has no matching entry in the target vocabulary; recorded as 'other' with the paper's own label.
  • exposures[2].target.termsParietal operculum (POp) has no matching entry in the target vocabulary; recorded as 'other' with the paper's own label.