Low dimensional criticality embedded in high dimensional awake brain dynamics

Whether cortical neurons operate in a strongly or weakly correlated dynamical regime determines fundamental information processing capabilities and has fueled decades of debate. Here we offer a resolution of this debate; we show that two important dynamical regimes, typically considered incompatible, can coexist in the same local cortical circuit by separating them into two different subspaces. In awake mouse motor cortex, we find a low-dimensional subspace with large fluctuations consistent with criticality – a dynamical regime with moderate correlations and multi-scale information capacity and transmission. Orthogonal to this critical subspace, we find a high-dimensional subspace containing a desynchronized dynamical regime, which may optimize input discrimination. The critical subspace is apparent only at long timescales, which explains discrepancies among some previous studies. Using a computational model, we show that the emergence of a low-dimensional critical subspace at large timescale agrees with established theory of critical dynamics. Our results suggest that cortex leverages its high dimensionality to multiplex dynamical regimes across different subspaces.