Laminar evoked responses in mouse somatosensory cortex suggest a special role for deep layers in cortical complexity

• Published in: The European journal of neuroscience Vol. 59; no. 5; pp. 752 - 770
• Main Authors: Hönigsperger, Christoph, Storm, Johan F., Arena, Alessandro
• Format: Journal Article
• Language: English
• Published: France Wiley Subscription Services, Inc 01.03.2024
• Subjects: anaesthesia; Anesthesia; brain state; complexity; connectivity; Consciousness; Cortex (motor); cortical layers; EEG; Electrical stimuli; Firing pattern; Firing rate; Neural networks; PCI; Sevoflurane; Sleep and wakefulness; Somatosensory cortex; cortical layers; complexity; connectivity; consciousness; PCI; brain state; anaesthesia
• ISSN: 0953-816X; 1460-9568
• DOI: 10.1111/ejn.16108

It has been suggested that consciousness is closely related to the complexity of the brain. 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 is unclear how different cortical layers respond to CS and contribute to the resulting intra‐ and inter‐areal cortical connectivity and PCI. A detailed investigation of the local dynamics is needed to understand the basis for PCI. We hypothesized that the complexity level of global cortical responses (PCI) correlates with layer‐specific activity and connectivity. We tested this idea by measuring global cortical dynamics and layer‐specific activity in the somatosensory cortex (S1) of mice, combining cortical electrical stimulation in deep motor cortex, global electrocorticography (ECoG) and local laminar recordings from layers 1–6 in S1, during wakefulness and general anaesthesia (sevoflurane). We found that the transition from wake to sevoflurane anaesthesia correlated with a drop in both the global and local PCI (PCIst) 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 changes in the state of consciousness. The brain's ability to engage in diversified and integrated neuronal responses is closely related to its conscious state. We show that anaesthesia is associated with drop in both intra‐cortical and intra‐laminar complexity following intracranial cortical stimulation. Deep layers 6 and 5 exhibit connectivity with remote cortical areas during wakefulness but not anaesthesia. Layer 6 shows the strongest modulation of spike firing and spike field coherence during wakefulness.