Abstract
During slow-wave sleep, the brain is in a self-organized regime in which slow oscillations (SOs) between up- and down-states travel across the cortex. While an isolated piece of cortex can produce SOs, the brain-wide propagation of these oscillations are thought to be mediated by the long-range axonal connections. We address the mechanism of how SOs emerge and recruit large parts of the brain using a whole-brain model constructed from empirical connectivity data in which SOs are induced independently in each brain area by a local adaptation mechanism. Using an evolutionary optimization approach, good fits to human resting-state fMRI data and sleep EEG data are found at values of the adaptation strength close to a bifurcation where the model produces a balance between local and global SOs with realistic spatiotemporal statistics. Local oscillations are more frequent, last shorter, and have a lower amplitude. Global oscillations spread as waves of silence across the undirected brain graph, traveling from anterior to posterior regions. These traveling waves are caused by heterogeneities in the brain network in which the connection strengths between brain areas determine which areas transition to a down-state first, and thus initiate traveling waves across the cortex. Our results demonstrate the utility of whole-brain models for explaining the origin of large-scale cortical oscillations and how they are shaped by the connectome.
Highlights
Slow oscillations (SOs) are a hallmark of slow-wave sleep (SWS), during which neuronal activity slowly (< 1 Hz) transitions between up-states of sustained firing and down-states in which the neurons remain almost completely silent (Steriade et al, 1993; Neske, 2016)
Our results demonstrate the utility of whole-brain models for representing a wider range of brain dynamics beyond the restingstate, which highlights their potential for elucidating the origin and the dynamical properties of large-scale brain oscillations in general
A whole-brain network model is constructed by combining a model of an isolated cortical region with information regarding the structural connectivity of the human brain (Figure 1)
Summary
Slow oscillations (SOs) are a hallmark of slow-wave sleep (SWS), during which neuronal activity slowly (< 1 Hz) transitions between up-states of sustained firing and down-states in which the neurons remain almost completely silent (Steriade et al, 1993; Neske, 2016). While the majority of SOs remain locally confined in a few brain regions, some can recruit the entire brain They preferably originate in anterior parts and propagate to posterior parts of the cortex, like a traveling wave (Massimini et al, 2004; Nir et al, 2011; Mitra et al, 2015; Malerba et al, 2019). In-vitro recordings of isolated cortical tissue (Sanchez-Vives and McCormick, 2000; Capone et al, 2019) demonstrate that SOs can be generated in the absence of any external neural inputs Taken together, these observations support the idea that SOs are generated locally in an individual brain region, while the synchronized propagation of SOs across the cortex is shaped by the global structure of the human connectome
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