Abstract
Slow cortical waves that propagate across the cerebral cortex forming large-scale spatiotemporal propagation patterns are a hallmark of non-REM sleep and anesthesia, but also occur during resting wakefulness. To investigate how the spatial temporal properties of slow waves change with the depth of anesthetic, we optically imaged population voltage transients generated by mouse layer 2/3 pyramidal neurons across one or two cortical hemispheres dorsally with a genetically encoded voltage indicator (GEVI). From deep barbiturate anesthesia to light barbiturate sedation, depolarizing wave events recruiting at least 50% of the imaged cortical area consistently appeared as a conserved repertoire of distinct wave motifs. Toward awakening, the incidence of individual motifs changed systematically (the motif propagating from visual to motor areas increased while that from somatosensory to visual areas decreased) and both local and global cortical dynamics accelerated. These findings highlight that functional endogenous interactions between distant cortical areas are not only constrained by anatomical connectivity, but can also be modulated by the brain state.
Highlights
Slow-wave sleep (SWS, referred to as non-REM sleep) is characterized by large-amplitude slow waves in the electroencephalogram (EEG; Blake, 1937)
We performed transcranial optical voltage imaging using the genetically encoded voltage indicator (GEVI) VSFP Butterfly 1.2 targeted to layer 2/3 pyramidal cells either via in utero electroporation (Akemann et al, 2010, 2012), imaging over one hemisphere, group 1; or using gene targeted mice based on the Cre-lox system (Madisen et al, 2015), imaging over both hemispheres, group 2
We developed an analysis strategy to identify and quantitatively characterize slow wave events transcranially imaged using a GEVI targeted to layer 2/3 cortical pyramidal neurons
Summary
Slow-wave sleep (SWS, referred to as non-REM sleep) is characterized by large-amplitude slow waves in the electroencephalogram (EEG; Blake, 1937). Cortical slow waves reflect the alternating transition between periods of neuronal hyperpolarization (silence state of cortical neuronal firing) and depolarization (active state of cortical neuronal firing; Steriade et al, 1993a,b,c, 2001; Cowan and Wilson, 1994; Contreras and Steriade, 1995; Timofeev et al, 2001; Chauvette et al, 2010) The alternation between these two distinct states of the cortical network, each lasting hundreds of milliseconds, results in a peak in the EEG and local field potential (LFP) power spectra in the range of 0.1–5 Hz. Intracellular recordings from anesthetized and awake rodents demonstrated that, when the LFP displays slow waves, neighboring cortical pyramidal neurons alternate between active and silent states synchronously (Crochet and Petersen, 2006; Mahon et al, 2006; Poulet and Petersen, 2008; Gentet et al, 2010; Okun et al, 2010). This synchronization can recruit cortical areas of variable sizes, generating local or global slow waves that can propagate spatially
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