Abstract
Traveling patterns of neuronal activity—brain waves—have been observed across a breadth of neuronal recordings, states of awareness, and species, but their emergence in the human brain lacks a firm understanding. Here we analyze the complex nonlinear dynamics that emerge from modeling large-scale spontaneous neural activity on a whole-brain network derived from human tractography. We find a rich array of three-dimensional wave patterns, including traveling waves, spiral waves, sources, and sinks. These patterns are metastable, such that multiple spatiotemporal wave patterns are visited in sequence. Transitions between states correspond to reconfigurations of underlying phase flows, characterized by nonlinear instabilities. These metastable dynamics accord with empirical data from multiple imaging modalities, including electrical waves in cortical tissue, sequential spatiotemporal patterns in resting-state MEG data, and large-scale waves in human electrocorticography. By moving the study of functional networks from a spatially static to an inherently dynamic (wave-like) frame, our work unifies apparently diverse phenomena across functional neuroimaging modalities and makes specific predictions for further experimentation.
Highlights
Traveling patterns of neuronal activity—brain waves—have been observed across a breadth of neuronal recordings, states of awareness, and species, but their emergence in the human brain lacks a firm understanding
We modeled large-scale brain dynamics using a network of coupled neural masses[41,42,43,44,45]
We describe the local dynamics of each brain region with a conductance-based neural mass[46]
Summary
Traveling patterns of neuronal activity—brain waves—have been observed across a breadth of neuronal recordings, states of awareness, and species, but their emergence in the human brain lacks a firm understanding. Transitions between states correspond to reconfigurations of underlying phase flows, characterized by nonlinear instabilities These metastable dynamics accord with empirical data from multiple imaging modalities, including electrical waves in cortical tissue, sequential spatiotemporal patterns in resting-state MEG data, and large-scale waves in human electrocorticography. A diversity of neuronal wave patterns have been observed on mesoscopic[8,9,10,11,12] and whole-brain scales[4,13,14,15] These waves are not merely epiphenomena: e.g., they have been reproducibly observed in visual processing16—carrying the primary stimulus-evoked response in visual cortex[8,17]; reflecting information flow in response to dynamic natural scenes[18]; encoding directions of moving stimuli[19]; encoding stimulus positions and orientations[20]; underlying bistable perceptual rivalry[21]; reinforcing recent visual experience[22]; and occur pathologically during visual hallucinations[23]. The presence of these waves does not depend upon the choice of neural model and is replicated on two independent whole-brain connectomes
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