The human brain mechanisms of afterimages: From networks to cortical layers

Abstract

Afterimages are common visual illusions that have long attracted popular and scientific interest, yet their neural mechanisms remain little understood. We used high-spatial-resolution fMRI to investigate human whole brain and cortical layer activity in primary visual cortex (V1) linked with afterimages and perceptually similar animated images - stimuli designed to imitate the appearance of afterimages. Both afterimages and perceptually similar images engaged overlapping, widespread brain activity, particularly in visual sensory regions that follow the contralateral circuitry of the primary visual pathway. However, afterimages elicited weaker fMRI signals across the brain compared to images, except in salience network regions, where activity was enhanced for afterimages. Salience network activity could reflect conflict or perceptual reality monitoring mechanisms that detect the illusory nature of afterimages. Cortical layer-specific analyses in V1 revealed afterimages selectively engaged middle and deep cortical layers, while perceptually similar images activated middle and superficial layers. In agreement, layer-specific decoding of afterimage and mock afterimage fMRI signals was present only in deep layers. One interpretation of these V1 cortical layer findings is that afterimage perception involves feedback or top-down neural input akin to self-generated or endogenous conscious perception (e.g., visual imagery). In addition, baseline eye behavior (pupil size and blinking) and fMRI signals in arousal, salience, and visual networks differed depending on whether afterimages were perceived or not perceived. These results challenge the prevailing framing on the neurophysiological origins of afterimages as arising from either retinal or central neural processes. As with image perception, typical afterimages emerge by the interaction between retinal and central neural mechanisms. These findings on the neural processing underlying afterimages may be broadly informative of the neural mechanisms of visual consciousness.