The Temporal Stability of Visual Cortical Processing in Humans Depends on Early Experience

Abstract

Proper timing is essential for effective neural processing. Yet, how early postnatal vision shapes the temporal stability of human visual cortical processing remains unknown. Here, using electroencephalography, we examined cortical timing properties in individuals who were born pattern vision blind due to congenital cataracts, but surgically recovered sight. While sight-recovery individuals exhibited an attenuated cortical oscillatory phase coherence (i.e., higher temporal variability) during visual processing, their oscillatory strength was unimpaired. Moreover, phase coherence information, but not activation strength, allowed the classification of sight-recovery from control individuals. Finally, exchanging phase information between sight-recovery and control individuals indicated oscillatory timing impairments as the source of group differences in higher-order visual cortical processing. Neural timing impairments were specific for reversed congenital blindness, that is, were not observed in individuals with reversed developmental (late-onset) cataracts. These results suggest that the development of intricately temporally orchestrated visual cortical processing in humans requires early visual experience. Significance StatementNeural circuit functioning requires an efficient temporal orchestration. The present work investigated how the temporal stability of visual cortical dynamics depends on adequate experience. In rare individuals who were born with pattern vision blindness but later recovered sight, a marked increase in the temporal variability of oscillatory brain activity during visual processing was observed while oscillatory strength was surprisingly unimpaired. Therefore, the emergence of precisely timed visual processing in the human brain seems to crucially depend on early visual experience. We speculate that impaired timing of neural processing, cascading throughout the visual cortical hierarchy, might be a major source of the incomplete visual recovery in individuals with treated congenital blindness.