The direction and timing of theta and alpha traveling waves modulate human memory processing

Abstract

To support a range of behaviors, the brain must flexibly coordinate neural activity across widespread brain regions. One potential mechanism for this coordination is a traveling wave, in which a neural oscillation propagates across the brain while organizing the order and timing of activity across regions (Ermentrout & Kleinfeld, 2001; Muller et al., 2018). Although traveling waves are present across the brain in various species (Lubenov & Siapas, 2009; Zhang et al., 2018; Davis et al., 2020), their potential functional relevance remained unknown. Here, using rare direct human brain recordings, we demonstrate two novel functional roles for traveling waves of theta- and alpha-band (2-13 Hz) oscillations in the cortex. First, traveling waves propagate in different directions during separate cognitive processes. In episodic memory, traveling waves tended to propagate in posterior-to-anterior and anterior-to-posterior directions, respectively, during encoding and retrieval. Second, traveling waves are informative about the timing of behavior, with the phase of ongoing traveling waves indicating when subjects would retrieve memories. Because traveling waves of oscillations correspond to local neuronal spiking, these patterns indicate that rhythmic pulses of activity move across the brain with different directions and timing for separate behaviors. More broadly, our results suggest a fundamental role for traveling waves and oscillations in dynamically coordinating neural connectivity, by flexibly organizing the timing and directionality of network interactions across the cortex to support cognition and behavior.

How can we detect and analyze traveling waves in human brain oscillations?

“…Furthermore, the timing (or phase) of traveling waves also plays a critical role in human cognition. In our recent study, we have shown that the timing of a wave precisely defines fast and slow response times, in a working memory task (51). These results may be similar to a set of findings in animals, where the phase of traveling beta oscillations predicted stimulus detection in visual perception (17).…”

“…Given that we found evidence for the existence of traveling waves across several frequency bands such as the delta, theta, alpha, and beta ranges (14,15,43,51), it raises an important question of how the waves in these bands relate to each other. Previous studies have shown that theta and beta traveling waves in the human insula travel independently of each other during resting-state (43).…”

“…Moreover, several features of traveling waves can be directly extracted from the parameters of our circular-linear regression model. We can then analyze the relationship of these features to different human behaviors as we have done in our previous studies (14,15,43,51).…”

“…More importantly, several studies have found that the propagation direction of these waves is linked to human behavior. The directions of traveling waves can distinguish speech compared to non-speech trials (11), successful memory encoding compared to unsuccessful memory encoding and memory recall in a verbal episodic memory task (51), and fast response times compared to slow response times in a working memory task (15), demonstrating its behavior relevance. Moreover, the directions of traveling waves also shift across brain regions.…”

“…Other studies have also shown that these traveling waves are also highly relevant for memory processing in the human brain, and not just in restingstate. Specifically these studies have shown a crucial role for theta and alpha oscillatory traveling waves during a working memory task (15) and also verbal episodic memory task (51), suggesting that lower frequency oscillations might be more relevant for memory processing in the human brain. Some other studies have also shown a role of low frequency delta, theta, and alpha oscillatory traveling waves during speech processing as well (11).…”