Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
Kianoush Banaie Boroujeni, Michelle K. Sigona, Robert Louie Treuting, Thomas J. Manuel, Charles F. Caskey, Thilo Womelsdorf
PLOS Biology 2022, 20, e3001785 · 10.1371/journal.pbio.3001785
Abstract
Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information sampling and biasing choices toward relevant objects, but they might also have indirect motivational functions by enabling subjects to estimate the value of putting effort into choosing objects. Here, we tested these possibilities by modulating neuronal activity in ACC and STR of nonhuman primates using transcranial ultrasound stimulation while subjects learned the relevance of objects in situations with varying motivational and cognitive demands. Motivational demand was indexed by varying gains and losses during learning, while cognitive demand was varied by increasing the uncertainty about which object features could be relevant during learning. We found that ultrasound stimulation of the ACC, but not the STR, reduced learning efficiency and prolonged information sampling when the task required averting losses and motivational demands were high. Reduced learning efficiency was particularly evident at higher cognitive demands and when subjects experienced loss of already attained tokens. These results suggest that the ACC supports flexible learning of feature values when loss experiences impose a motivational challenge and when uncertainty about the relevance of objects is high. Taken together, these findings provide causal evidence that the ACC facilitates resource allocation and improves visual information sampling during adaptive behavior.
Abstract via europepmc.
Exposures
Exposure 1: TUS to ACC (area 24)
Target: dorsal anterior cingulate cortex — “ACC (area 24)”
Device: Sonic Concepts · Sonic Concepts · H115MR ✓
| 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) | 1,200 | ✓✓✓ |
|---|---|---|
| Free-field Isppa (W/cm²) | not reported | |
| Free-field Ispta (W/cm²) | not reported | |
| In-situ estimate | not reported | |
| In-situ pressure (kPa) | not reported | |
| In-situ Isppa (W/cm²) | not reported | |
| In-situ Ispta (W/cm²) | not reported |
30-ms bursts of TUS were delivered every 100 ms over a duration of 80 seconds (40 seconds each hemisphere). We bilaterally sonicated or sham-sonicated the ACC or the STR in individual sessions immediately after monkeys had completed the first 6 learning blocks.
Exposure 2: TUS to anterior striatum (head of caudate)
Target: caudate nucleus — “anterior striatum (STR, head of the caudate nucleus)”
Device: Sonic Concepts · Sonic Concepts · H115MR ✓
| 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) | 1,200 | ✓✓✓ |
|---|---|---|
| Free-field Isppa (W/cm²) | not reported | |
| Free-field Ispta (W/cm²) | not reported | |
| In-situ estimate | not reported | |
| In-situ pressure (kPa) | not reported | |
| In-situ Isppa (W/cm²) | not reported | |
| In-situ Ispta (W/cm²) | not reported |
30-ms bursts of TUS were delivered every 100 ms over a duration of 80 seconds (40 seconds each hemisphere). We bilaterally sonicated or sham-sonicated the ACC or the STR in individual sessions immediately after monkeys had completed the first 6 learning blocks.
Flags from extraction
exposures[0].unspecified_domain.pressure_kpa— 1.2 MPa pressure is stated for the stimulation protocol but the sentence does not explicitly say whether it is a free-field or in-situ value; the following sentences describe hydrophone calibration in water, so domain is ambiguous and the value is placed in unspecified_domain.exposures[1].unspecified_domain.pressure_kpa— Same 1.2 MPa value and domain ambiguity as exposures[0]; same protocol used for both targets.exposures[0].timing.pulse_repetition_frequency_hz— PRF (10 Hz) converted from the stated inter-burst interval of 100 ms; not stated directly as Hz in the text.exposures[1].timing.pulse_repetition_frequency_hz— PRF (10 Hz) converted from the stated inter-burst interval of 100 ms; not stated directly as Hz in the text.exposures[0].timing.duty_cycle_pct— Duty cycle not stated by the paper; leaving not_reported rather than computing from pulse duration (30 ms) and period (100 ms).direction_of_effect— Direction is inferred from behavioural impairment only; no direct neural recording of ACC activity was performed in this study.