The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change
Elsa F. Fouragnan, Bolton K. H. Chau, Davide Folloni, Nils Kolling, Lennart Verhagen, Miriam Klein-Flügge, Lev Tankelevitch, Georgios K. Papageorgiou, Jean-Francois Aubry, Jerome Sallet, Matthew F. S. Rushworth
Nature Neuroscience 2019 · 10.1038/s41593-019-0375-6
Abstract
The neural mechanisms mediating sensory-guided decision-making have received considerable attention, but animals often pursue behaviors for which there is currently no sensory evidence. Such behaviors are guided by internal representations of choice values that have to be maintained even when these choices are unavailable. We investigated how four macaque monkeys maintained representations of the value of counterfactual choices-choices that could not be taken at the current moment but which could be taken in the future. Using functional magnetic resonance imaging, we found two different patterns of activity co-varying with values of counterfactual choices in a circuit spanning the hippocampus, the anterior lateral prefrontal cortex and the anterior cingulate cortex. Anterior cingulate cortex activity also reflected whether the internal value representations would be translated into actual behavioral change. To establish the causal importance of the anterior cingulate cortex for this translation process, we used a novel technique, transcranial focused ultrasound stimulation, to reversibly disrupt anterior cingulate cortex activity.
Abstract via europepmc.
Exposures
Exposure 1: TUS of anterior cingulate cortex (ACC)
Target: anterior cingulate cortex — “anterior cingulate cortex (ACC)”
Device: Sonic Concepts · Sonic Concept · H115-MR ✓
| Waveform | pulsed | |
|---|---|---|
| Fundamental frequency (kHz) | 250 | ✓✓✓ |
| Pulse duration (ms) | 30 | ✓✓✓ |
| Pulse repetition frequency (Hz) | 10 | ✓✓✓ |
| Duty cycle (%) | not reportedpulse duration × PRF gives 30% | ⚑ |
| Sonication duration (s) | 40 | ✓✓✓ |
| Free-field pressure (kPa) | 1,152, 1,292swept | ✓✓✓ |
|---|---|---|
| Free-field Isppa (W/cm²) | not reported | |
| Free-field Ispta (W/cm²) | not reported | |
| In-situ estimate | deratingsingle value | |
| In-situ pressure (kPa) | 760, 850swept | ✓✓✓⚑ |
| In-situ Isppa (W/cm²) | not reported | |
| In-situ Ispta (W/cm²) | not reported |
30 ms bursts of 250 kHz ultrasound generated every 100 ms; the stimulation lasted 40 s overall, applied immediately before testing (or before rs-fMRI).
Exposure 2: TUS of lateral orbitofrontal cortex (lOFC)
Target: orbitofrontal cortex — “lateral orbitofrontal cortex (lOFC)”
Device: Sonic Concepts · Sonic Concept · H115-MR ✓
| Waveform | pulsed | |
|---|---|---|
| Fundamental frequency (kHz) | 250 | ✓✓✓ |
| Pulse duration (ms) | 30 | ✓✓✓ |
| Pulse repetition frequency (Hz) | 10 | ✓✓✓ |
| Duty cycle (%) | not reportedpulse duration × PRF gives 30% | |
| Sonication duration (s) | 40 | ✓✓✓ |
| Free-field pressure (kPa) | 1,152, 1,292swept | ✓✓✓ |
|---|---|---|
| Free-field Isppa (W/cm²) | not reported | |
| Free-field Ispta (W/cm²) | not reported | |
| In-situ estimate | deratingsingle value | |
| In-situ pressure (kPa) | 760, 850swept | ✓✓✓ |
| In-situ Isppa (W/cm²) | not reported | |
| In-situ Ispta (W/cm²) | not reported |
30 ms bursts of 250 kHz ultrasound generated every 100 ms; the stimulation lasted 40 s overall, applied immediately before testing (or before rs-fMRI).
Flags from extraction
n_subjects— Four animals received TUS in total (two ACC and four lOFC); rs-fMRI TUS data from one animal; four animals contributed fMRI without TUS.n_sessions_per_subject— Nine ACC-TUS sessions in each of two animals; lOFC had 5 sessions per animal (4 animals x 5); ACC value recorded.exposures[1].timing— lOFC protocol stated to use the same design as ACC-TUS; parameters assumed identical because the paper describes one TUS protocol.exposures[0].timing.duty_cycle_pct— Duty cycle not stated.exposures[0].in_situ.pressure_kpa— Derated by the authors using a mean 66% skull transmission from the literature, not measured in these animals; range reflects session voltages.direction_of_effect— TUS described as disrupting ACC activity; effect direction on neural activity not clearly excitatory or inhibitory.anaesthesia— Behavioural testing in awake animals; rs-fMRI under isoflurane.randomised— Day order described as pseudorandom, counterbalanced; sham sessions interleaved.