Cortex-wide spatiotemporal motifs of theta oscillations are coupled to freely moving behavior

Abstract

Multisensory information is combined across the cortex and assimilated into the continuous production of ongoing behavior. In the hippocampus, theta oscillations (4-12 Hz) radiate as large-scale traveling waves, and serve as a scaffold for neuronal ensembles of multisensory information involved in memory and movement-related processing. An extension of such an encoding framework across the neocortex could similarly serve to bind disparate multisensory signals into ongoing, coherent, phase-coded processes. Whether the neocortex exhibits unique large-scale traveling waves distinct from that of the hippocampus however, remains unknown. Here, using cortex-wide electrocorticography in freely moving mice, we find that theta oscillations are organized into bilaterally-symmetric spatiotemporal "modes" that span virtually the entire neocortex. The dominant mode (Mode 1) is a divergent traveling wave that originates from retrosplenial cortex and whose amplitude correlates with mouse speed. Secondary modes are asynchronous spiral waves centered over primary somatosensory cortex (Modes 2 & 3), which become prominent during rapid drops in amplitude and synchrony (null spikes) and which underlie a phase reset of Mode 1. These structured cortex-wide traveling waves may provide a scaffold for large-scale phase-coding that allows the binding of multisensory information across all the regions of the cortex. Bulleted list of key resultsO_LICortical theta oscillations are organized into bilaterally-symmetric spatiotemporal modes that span the neocortex. C_LIO_LIThe dominant mode appears as a divergent traveling wave that originates in retrosplenial cortex and is correlated with mouse speed. C_LIO_LISecondary modes are asynchronous spiral waves centered over somatosensory cortex. C_LIO_LISecondary modes become prominent during transient drops in synchrony that underlie a phase reset of the dominant mode. C_LIO_LIWe hypothesize that spiral waves may provide a mechanism to exert large-scale phase separability, and assimilate information into ongoing multisensory processing across the neocortex. C_LI