The Human Brain Encodes a Chronicle of Visual Events at Each Instant of Time Through the Multiplexing of Traveling Waves

Abstract

The human brain continuously processes streams of visual input. Yet, a single image typically triggers neural responses that extend beyond 1s. To understand how the brain encodes and maintains successive images, we analyzed with electroencephalography the brain activity of human subjects while they watched ∼5000 visual stimuli presented in fast sequences. First, we confirm that each stimulus can be decoded from brain activity for ∼1s, and we demonstrate that the brain simultaneously represents multiple images at each time instant. Second, we source localize the corresponding brain responses in the expected visual hierarchy and show that distinct brain regions represent, at each time instant, different snapshots of past stimulations. Third, we propose a simple framework to further characterize the dynamical system of these traveling waves. Our results show that a chain of neural circuits, which each consist of (1) a hidden maintenance mechanism and (2) an observable update mechanism, accounts for the dynamics of macroscopic brain representations elicited by visual sequences. Together, these results detail a simple architecture explaining how successive visual events and their respective timings can be simultaneously represented in the brain.

SIGNIFICANCE STATEMENT Our retinas are continuously bombarded with a rich flux of visual input. Yet, how our brain continuously processes such visual streams is a major challenge to neuroscience. Here, we developed techniques to decode and track, from human brain activity, multiple images flashed in rapid succession. Our results show that the brain simultaneously represents multiple successive images at each time instant by multiplexing them along a neural cascade. Dynamical modeling shows that these results can be explained by a hierarchy of neural assemblies that continuously propagate multiple visual contents. Overall, this study sheds new light on the biological basis of our visual experience.