Turning the Stimulus On and Off Changes the Direction of α Traveling Waves

Abstract

Traveling waves have been studied to characterize the complex spatiotemporal dynamics of the brain. Several studies have suggested that the propagation direction of α traveling waves can be task dependent. For example, a recent electroencephalography (EEG) study from our group found that forward waves (i.e., occipital to frontal, FW waves) were observed during visual processing, whereas backward waves (i.e., frontal to occipital, BW waves) mostly occurred in the absence of sensory input. These EEG recordings, however, were obtained from different experimental sessions and different groups of subjects. To further examine how the waves’ direction changes between task conditions, 13 human participants were tested on a target detection task while EEG signals were recorded simultaneously. We alternated visual stimulation (5-s display of visual luminance sequences) and resting state (5 s of black screen) within each single trial, allowing us to monitor the moment-to-moment progression of traveling waves. As expected, the direction of α waves was closely linked with task conditions. First, FW waves from occipital to frontal regions, absent during rest, emerged as a result of visual processing, while BW waves in the opposite direction dominated in the absence of visual inputs, and were reduced (but not eliminated) by external visual inputs. Second, during visual stimulation (but not rest), both waves coexisted on average, but were negatively correlated. In summary, we conclude that the functional role of α traveling waves is closely related with their propagating direction, with stimulus-evoked FW waves supporting visual processing and spontaneous BW waves involved more in top-down control.

Distinct roles of forward and backward alpha-band waves in spatial visual attention

“…All in all, we could confirm our previous conclusion that covert visual attention modulates top-down oscillatory waves, showing this effect even in the absence of visual stimulation. In addition, we surmised that the lateralization effect we reported in the forward waves in our dataset (absent in the Foster dataset) is related to the steady visual stimulation during the attentional allocation, in line with our previous results demonstrating that oscillatory bottom-up waves reflect sensory processing ( Alamia and VanRullen, 2019 ; Pang et al, 2020 ).…”

“…However, before testing how visual attention modulates traveling waves, we explored the amount of waves propagating forward (FW) and backward (BW) as a function of their temporal frequency (see Figure 5 and methods for a detailed description of the analysis). Figure 1D shows the spectral profile of FW and BW waves in the midline (along the Oz–Fz axis) and the contra- and ipsilateral lines: confirming previous experimental studies ( Alamia and VanRullen, 2019 ; Pang et al, 2020 ), we found that alpha-band oscillatory waves propagate in both directions during visual stimulation, whereas theta (4–7 Hz) and high-beta/gamma (24–45 Hz) bands propagate mostly bottom-up from occipital to frontal regions, and low-beta (13–23 Hz) waves flow in the top-down direction. Interestingly, this pattern of results confirms previous studies using different methods, in which higher frequency bands (i.e., high-beta/gamma) have been associated with forward processing, whereas low-beta and alpha frequencies have been related to top-down processing ( Bastos et al, 2012 ; Bastos et al, 2015 ; van Kerkoerle et al, 2014 ; Michalareas et al, 2016 ; but see also Schneider et al, 2021b ).…”

“…Here, we took a novel perspective on these results by interpreting oscillations as traveling waves ( Muller et al, 2018 ), thus considering their spatial component on top of the temporal one. Our results revealed two distinct alpha-band waves propagating in opposite directions: attention modulates oscillations traveling from occipital to frontal regions only in the presence of visual stimulation, thus relating forward waves to visual processing ( Lozano-Soldevilla and VanRullen, 2019 ; Pang et al, 2020 ); whereas oscillations propagating in the opposite, top-down direction were modulated by attention irrespective of the presence or absence of concurrent visual stimulation; as in standard studies of alpha power lateralization ( Worden et al, 2000 ; Sauseng et al, 2005 ; Kelly et al, 2006 ; Thut et al, 2006 ; Händel et al, 2011 ), this attentional modulation involved both an decrease of alpha waves contralateral to the attended location, and an ipsilateral increase.…”

“…Considering the case of visual attention, we tested the hypothesis that two functionally distinct alpha-band oscillations propagate along the frontal–occipital line in opposite directions. This compelling hypothesis about the different functional roles of alpha-band traveling waves derives from our previous studies ( Alamia and VanRullen, 2019 ; Pang et al, 2020 ), in which we showed how visual perception modulates alpha waves, that is forward waves during visual stimulation, backward waves when the stimulus was off. In addition, this hypothesis is in line with previous studies suggesting that distinct alpha-band oscillations are related to specific cognitive processes ( Gulbinaite et al, 2017 ; Deng et al, 2019 ; Schuhmann et al, 2019 ; Sokoliuk et al, 2019 ; Kasten et al, 2020 ).…”

“…Another highly replicated result regarding the inhibitory role of alpha oscillations consists in the hemispheric modulation in occipital regions associated with visual attention, having an increase of power ipsilateral to the attended hemifield, and a corresponding decrease contralaterally ( Worden et al, 2000 ; Sauseng et al, 2005 ; Kelly et al, 2006 ; Thut et al, 2006 ; Händel et al, 2011 ). On the other hand, other experimental studies have related alpha-band oscillations in occipital and parietal regions to perceptual processing and visual memory ( Bonnefond and Jensen, 2012 ; VanRullen, 2016 ; Pang et al, 2020 ; Luo et al, 2021 ). For example, reverse-correlation techniques reveal that the visual system reverberates sensory information in the alpha-band for as long as 1 s, in what has been dubbed ‘perceptual echoes’ ( VanRullen and Macdonald, 2012 ).…”