Traveling waves and trial averaging: The nature of single-trial and averaged brain responses in large-scale cortical signals

Abstract

Analyzing single trial brain activity remains a challenging problem in the neurosciences. We gain purchase on this problem by focusing on globally synchronous fields in within-trial evoked brain activity, rather than on localized peaks in the trial-averaged evoked response (ER). We analyzed data from three measurement modalities, each with different spatial resolutions: magnetoencephalogram (MEG), electroencephalogram (EEG) and electrocorticogram (ECoG). We first characterized the ER in terms of summation of phase and amplitude components over trials. Both contributed to the ER, as expected, but the ER topography was dominated by the phase component. This means the observed topography of cross-trial phase will not necessarily reflect the phase topography within trials. To assess the organization of within-trial phase, traveling wave (TW) components were quantified by computing the phase gradient. TWs were intermittent but ubiquitous in the within-trial evoked brain activity. At most task-relevant times and frequencies, the within-trial phase topography was described better by a TW than by the trial-average of phase. The trial-average of the TW components also reproduced the topography of the ER; we suggest that the ER topography arises, in large part, as an average over TW behaviors. These findings were consistent across the three measurement modalities. We conclude that, while phase is critical to understanding the topography of event-related activity, the preliminary step of collating cortical signals across trials can obscure the TW components in brain activity and lead to an underestimation of the coherent motion of cortical fields.

Combining EEG and eye movement recording in free viewing: Pitfalls and possibilities

“…On the other hand, reliable estimation of evoked potentials is possible only after averaging of many trials. In the averaging, task-relevant information may be lost (Alexander et al, 2013(Alexander et al, , 2015. In contrast, the time-frequency analysis can reliably be done on single trials, which allows to study how experimental stimulation modulates ongoing brain activity.…”

A temporo-spatial analysis of the neural correlates of extrinsic perceptual grouping in vision

“…In this direction, the results of a study by Alexander et al (2013), suggested that phase topography and phase gradient, rather than trial average, may be more relevant to the understanding of event-related activity. The use of similar methodological approaches may provide a promising tool for future research in order to further characterize the neural mechanisms involved in perceptual grouping.…”

Propagating Neocortical Gamma Bursts Are Coordinated by Traveling Alpha Waves

“…Traveling waves have also been observed in the scalp EEG, although there is some debate as to whether it reflects the propagation of cortical activity or if it can be explained by volume conduction of the activity from a few neuronal sources (Hughes, 1995;Nunez et al, 2001;Alexander et al, 2013). Recent work has demonstrated cross-frequency interactions in which the amplitude of gamma band activity is coupled to the phase of alpha activity (Osipova et al, 2008;Voytek et al, 2010;Spaak et al, 2012).…”