Playing at the Edge of Criticality: Expanded Whole-Brain Repertoire of Connectome-Harmonics

In order for us to survive, our behaviour has to be perched somewhere between stability and flexibility, or between exploitation and exploration of available resources. This requires the underlying spatiotemporal brain dynamics to be delicately balanced between order and disorder, drawing upon a large repertoire of available brain states. Beyond survival, in order to thrive the brain has to be sufficiently flexible to be able to seek novel trajectories and expand the dynamical repertoire. Here we propose that a key ingredient could be play, the active exploration of novelty beyond exploiting existing potentially scarce resources. Using a novel analysis method called ‘connectome harmonics’ we not only demonstrate that brain activity resides close to criticality—at the delicate balance between order (stability) and disorder (flexibility)—but this whole-brain criticality is also intrinsically linked to oscillatory brain dynamics. We show that compared to wakefulness, other conscious states are related to different connectome-harmonic repertoires and differ in their proximity to criticality, where the critical regime may enhance the ability to flexibly seek new brain states. In particular, we propose that these brain dynamics may underlie the creative process found in play and improvisation, and as such may shed new light on discovering how the brain optimizes the balance between exploitation and exploration needed for behavioural flexibility.