Probing the edge of synchronization: Slow waves erode resting activity in behaving monkeys

Brain networks oscillate between sleep and wakefulness, following circadian rhythms. Theoretical models suggest distinct phases within this cycle, separated by a critical point where long-range activity patterns emerge, an advantageous condition for information processing in cortical networks. However, the exact nature of this critical dynamics remains elusive. A key question is whether the brain operates at this critical point during cognitive tasks or only during resting wakefulness. Here, we analyzed neural signals from the premotor cortex (PMC) of two macaque monkeys engaged in a delayed-reaching task and under drug-induced unconsciousness. We found evidence of criticality during resting periods at the end of behavioral trials in the awake state. This scale-free activity appeared as coordinated traveling waves, like those observed during anesthesia. As predicted by spiking networks models, activity-dependent adaptation influences wave size, supporting the hypothesis that the PMC operates near a synchronization phase transition while avoiding it during active behaviors.