Light modulates oscillatory alpha activity in the occipital cortex of totally visually blind individuals with intact non-image-forming photoreception

Abstract

The discovery of intrinsically photosensitive retinal ganglion cells (ipRGCs) marked a major shift in our understanding of how light information is processed by the mammalian brain. These ipRGCs influence multiple functions not directly related to image formation such as circadian resetting and entrainment, pupil constriction, enhancement of alertness, as well as the modulation of cognition. More recently, it was demonstrated that ipRGCs may also contribute to basic visual functions. The impact of ipRGCs on visual function, independently of image forming photoreceptors, remains difficult to isolate, however, particularly in humans. We previously showed that exposure to intense monochromatic blue light (465 nm) induced non-conscious light perception in a forced choice task in three rare totally visually blind individuals without detectable rod and cone function, but who retained non-image-forming responses to light, very likely via ipRGCs. The neural foundation of such light perception in the absence of conscious vision is unknown, however. In this study, we characterized the brain activity of these three participants using electroencephalography (EEG), and demonstrate that unconsciously perceived light triggers an early and reliable transient desynchronization (i.e. decreased power) of the alpha EEG rhythm (8-14 Hz) over the occipital cortex. These results provide compelling insight into how ipRGC may contribute to transient changes in ongoing brain activity. They suggest that occipital alpha rhythm synchrony, which is typically linked to the visual system, is modulated by ipRGCs photoreception; a process that may contribute to the non-conscious light perception in those blind individuals.

Figure 1

Desynchronization of the occipital alpha/low beta rhythm during 10 second stimulation with blue light in three blind participants with intact non-image-forming photoreception. (A) Frequency spectra for the entire 10 s period of blue light (blue), and darkness (black) show differences between conditions in all three participants (horizontal gray bar, p < 0.05, permutation-cluster-corrected for multiple comparisons) for the frequency band of interest (shaded area, 8–14 Hz). (B) Source reconstructions depict the difference between conditions (thresholded at p < 0.05, FDR corrected for multiple comparisons), at the individual alpha frequency showing greatest light-induced decrease (see main text). Statistical maps (t-values) of the topographies with the absolute difference between conditions at the individual alpha frequencies show that the spatial extent of the decrease in alpha power is largely restricted to occipital lobe. (C) Time-frequency representations illustrate differences between the light-ON versus light-OFF condition in time. Open rectangles highlight the time range of greatest difference (p < 0.05, FDR-cluster-corrected for multiple comparisons).

Figure 2

Conjunction analysis across the source statistical maps identified an area in bilateral superior occipital gyrus and cuneus as a significant (p < 0.05) cortical source of the alpha suppression in response to blue light, common to all three participants.