Trial-by-trial variability in cortical responses exhibits scaling of spatial correlations predicted from critical dynamics

In the mammalian cortex, even simple sensory inputs or movements activate many neurons, with each neuron responding variably to repeated stimuli—a phenomenon known as trial-by-trial variability. Understanding the spatial patterns and dynamics of this variability is challenging. Using cellular 2-photon imaging, we study visual and auditory responses in the primary cortices of awake mice. We focus on how individual neurons’ responses differed from the overall population. We find consistent spatial correlations in these differences that are unique to each trial and linearly scale with the cortical area observed, a characteristic of critical dynamics as confirmed in our neuronal simulations. Using chronic multi-electrode recordings, we observe similar scaling in the prefrontal and premotor cortex of non-human primates during self-initiated and visually cued motor tasks. These results suggest that trial-by-trial variability, rather than being random noise, reflects a critical, fluctuation-dominated state in the cortex, supporting the brain's efficiency in processing information.