State-dependent intrinsic predictability of cortical network dynamics

The information encoded in cortical circuit dynamics is fleeting, changing from moment to moment as new input arrives and ongoing intracortical interactions progress. A combination of deterministic and stochastic biophysical mechanisms governs how cortical dynamics at one moment evolve from cortical dynamics in recently preceding moments. Such temporal continuity of cortical dynamics is fundamental to many aspects of cortex function but is not well understood. Here we study temporal continuity by attempting to predict cortical population dynamics (multisite local field potential) based on its own recent history in somatosensory cortex of anesthetized rats and in a computational network-level model. We found that the intrinsic predictability of cortical dynamics was dependent on multiple factors including cortical state, synaptic inhibition, and how far into the future the prediction extends. By pharmacologically tuning synaptic inhibition, we obtained a continuum of cortical states with asynchronous population activity at one extreme and stronger, spatially extended synchrony at the other extreme. Intermediate between these extremes we observed evidence for a special regime of population dynamics called criticality. Predictability of the near future (10-100 ms) increased as the cortical state was tuned from asynchronous to synchronous. Predictability of the more distant future (> 1 s) was generally poor, but, surprisingly, was higher for asynchronous states compared to synchronous states. These experimental results were confirmed in a computational network model of spiking excitatory and inhibitory neurons. Our findings demonstrate that determinism and predictability of network dynamics depend on cortical state and the time-scale of the dynamics.