The hidden spatial dimension of alpha: 10 Hz perceptual echoes propagate as periodic travelling waves in the human brain.

Abstract

Alpha oscillations play a special role in vision. During sensory processing, reverse-correlation techniques revealed that white-noise luminance sequences elicit a robust occipital [~]10 Hz response that periodically reverberates the input sequence for up to 1 s. These perceptual echoes constitute the impulse response function of the visual system. However, the spatial dimension of perceptual echoes remains unknown: do they reverberate across the cortex simultaneously? Does stimulation over multiple visual coordinates evoke multiple synchronized echoes, or do they show consistent phase differences? Here, we tested the spatial dimension of perceptual echoes in two electroencephalogram (EEG) experiments manipulating the location of the visual stimulation. When a single disc flickered a white-noise luminance sequence in the upper visual field, we observed a single \"echo wave\" originating in posterior sensors and spatially propagating towards frontal ones (i.e. periodic travelling wave). The presentation of two independent flickering discs in separate visual hemifields produced two simultaneous and superimposed echo waves propagating in opposite directions, one in response to each stimulus. Strikingly, at many electrode sites, the phase of the two echoes differed, with a phase advance for the contralateral stimulus location. EEG source reconstruction tentatively located the waves within contralateral parieto-occipital cortex. In conclusion, the alpha rhythm processes stimulus information as a travelling wave that propagates across the cortical representation of retinotopic space in the human brain. In line with the \"cortical scanning\" hypothesis (Pitts & McCulloch, 1947), these results suggest the existence of an additional spatial dimension embedded in the phase of the alpha rhythm.\n\nSignificance statementHow does the spatial dimension of sensory processing relate to the temporal dimension of brain rhythms? Using correlation techniques, we characterized perceptual echoes, the average electroencephalogram response induced by visual stimuli that change luminance randomly. We found that perceptual echoes are actually periodic waves that travel through human visual cortex. Strikingly these periodic waves show consistent phase differences across the visual field, processing screen locations sequentially across distinct phases of the cycle following basic retinotopy. These results suggest the existence of an additional \"hidden\" spatial dimension in sensory cortex, encoded in the phase of the alpha oscillatory cycle. This could mean that perceptual echoes behave like sweeps of a sonar, processing the visual field in cycles of [~]100 ms duration.