Low frequency traveling waves in the human cortex coordinate neural activity across spatial scales

Abstract

Traveling waves of oscillatory activity are thought to influence neuronal spiking, providing a spatiotemporal frame-work for neural communication. However, no direct link has been established between traveling waves and single unit spiking in humans. We examined traveling waves in the human lateral temporal lobe by using recordings from intracranial electrodes implanted in twenty participants for seizure monitoring as they performed a paired-associates verbal memory task. We observed ubiquitous low frequency traveling waves across the temporal lobe. Long-range alpha waves were more likely to occur during word pairs that were subsequently remembered relative to those that were not. In a subset of participants with microelectrode recordings, macro-scale waves co-occurred with micro-scale waves, which in turn were temporally locked to single unit spiking. This temporal coordination between traveling waves at different spatial scales and between waves and neuronal spiking in the human brain suggests a role for traveling waves in neural communication.

Traveling waves in the prefrontal cortex during working memory

“…An example of a beta-band (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) wave during test screen presentation of one trial is shown in Fig 1C (S1 Movie). The tiles represent the electrodes in the array.…”

“…Traveling waves have most often been reported in the lower-frequency bands (<30 Hz). Examples include beta-band (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) traveling waves in motor and visual cortices [14,15] and theta band (3)(4)(5) traveling waves in the hippocampus [16,17].…”

“…Traveling waves are of interest because they have a variety of useful properties for cognition, development, and behavior. They can create timing relationships that foster spike-timingdependent plasticity and memory encoding [14,18]. They add information about recent history of activation of local networks [19].…”

Traveling waves in the prefrontal cortex during working memory

“…Traveling waves are of interest because they have a variety of useful properties for cognition, development, and behavior. They can create timing relationships that foster spike-timing-dependent plasticity and memory encoding (14,18). They add information about recent history of activation of local networks (19).…”

Spatiotemporal organization of human sensorimotor beta burst activity

“…The latter is thought to mirror proximal and distal sites within the motor cortex (Rubino et al, 2006), with proximal representations (i.e., shoulder and elbow) located more medially and distal representations (i.e., wrist and fingers) located more laterally (Penfield & Boldrey, 1937). This suggests that at a macro-scale level, the direction of wave propagation is dictated by the underlying horizontal connections, though further work across different spatial scales (such as (Sreekumar et al, 2020)) is required to fully unpack the precise relationship between sustained rhythmic synchronous spiking activity within neural populations, mesoscopic and macroscopic traveling wave activity.…”