The activity of deep cortical layers characterizes thecomplexity of brain responses during wakefulnessfollowing electrical stimulation

It has been suggested that the complexity of the brain is closely related to its state of consciousness. The perturbational complexity index (PCI) has been used in humans and rodents to distinguish conscious from unconscious states based on the global cortical responses (recorded by electroencephalography; EEG) to local cortical stimulation (CS). However, it has been unclear how different cortical layers respond to CS and contribute to the resulting intra- and inter-areal cortical communication and PCI. A detailed investigation of these local dynamics is needed to understand the basis for PCI. We hypothesized that the complexity level of global cortical responses (PCI) corresponds to variations in layer-specific activity and connectivity patterns. We investigated global cortical dynamics and layer specific activity in mice, combining cortical electrical stimulation, global EEG, and local multi-electrode, laminar recordings from layers 1-6 in somatosensory cortex, during wakefulness and general anesthesia (sevoflurane). We found that transition from wake to sevoflurane anesthesia correlated with a drop in global and local PCI values (complexity). This was accompanied by a local decrease in neural firing rate, spike-field coherence, and long-range functional connectivity specific to deep layers (L5, L6). Our results suggest that deep cortical layers are mechanistically important for changes in PCI, and thereby for variations in the states of consciousness. HighlightsO_LIAnesthesia caused a reduction in the perturbational complexity index (PCIST) at both global (inter-areal) and local (intra-areal, across layers) cortical scales. C_LIO_LIDeep cortical layers (L6 and L5), exhibited strong connectivity with remote cortical areas during wakefulness but not during anesthesia. C_LIO_LILayer 6 showed the strongest modulation of spike firing and spike field coherence compared to more superficial layers during wakefulness. C_LI