Cortical traveling waves link visual and frontal cortex during working memory-guided behavior

Abstract

Cortical traveling waves, or global patterns of activity that extend over several centimeters of the cortical surface, are a key mechanism for guiding the spatial propagation of neural activity and computational processes across the brain. Recent studies have implicated cortical traveling waves in successful short- and long-term memory encoding, storage, and retrieval. However, human memory systems are fundamentally-action oriented: eventually, the contents of memory must be utilized to produce appropriate behaviors. Cortical traveling waves could contribute to the production and control of memory-guided behaviors by flexibly routing information between brain areas responsible for storing memory content and brain areas responsible for planning and executing actions. Here, using short-term memory as a test case, we report evidence supporting this possibility. By applying image-based analyses to published human EEG studies, we show that the initiation of a memory-guided behavior is accompanied by a low-frequency (2-6 Hz) feedforward (occipital to frontal) traveling wave that predicts intra- and inter-individual differences in response onset, while the termination of a memory-guided behavior is followed by a higher frequency (14-32 Hz) feedback (frontal-to-occipital) traveling wave. Control analyses established that neither waveform could be explained by nuisance factors (e.g., propagation of visually-evoked potentials, eye movements, or passive volume conduction). Moreover, both waveforms required an overt behavior: when participants selected task-relevant memory content and prepared but did not yet execute an action based on this content, neither waveform was observed. Our findings suggest a role for traveling waves in the generation and control of memory-guided behaviors by flexibly organizing the timing and direction of interactions between brain regions involved in memory storage and action.