The avalanche-like behaviour of large-scale haemodynamic activity from wakefulness to deep sleep

Abstract

Increasing evidence suggests that responsiveness is associated with critical or near-critical cortical dynamics, which exhibit scale-free cascades of spatiotemporal activity. These cascades, or 'avalanches', have been detected at multiple scales, from in vitro and in vivo microcircuits to voltage imaging and brain-wide functional magnetic resonance imaging (fMRI) recordings. Criticality endows the cortex with certain information-processing capacities postulated as necessary for conscious wakefulness, yet it remains unknown how unresponsiveness impacts on the avalanche-like behaviour of large-scale human haemodynamic activity. We observed a scale-free hierarchy of co-activated connected clusters by applying a point-process transformation to fMRI data recorded during wakefulness and non-rapid eye movement (NREM) sleep. Maximum-likelihood estimates revealed a significant effect of sleep stage on the scaling parameters of the cluster size power-law distributions. Post hoc statistical tests showed that differences were maximal between wakefulness and N2 sleep. These results were robust against spatial coarse graining, fitting alternative statistical models and different point-process thresholds, and disappeared upon phase shuffling the fMRI time series. Evoked neural bistabilities preventing arousals during N2 sleep do not suffice to explain these differences, which point towards changes in the intrinsic dynamics of the brain that could be necessary to consolidate a state of deep unresponsiveness.