A Sensitive Period for the Development of Temporally Coherent Visual Cortical Processing in Humans: Evidence from Sight Recovery Following Congenital Cataracts

Typical cortical development requires early sensory experience. In humans who had suffered from a transient period of blindness due to dense bilateral congenital cataracts (CC), multiple investigations of cortical activation strength have suggested that extrastriate visual regions are especially vulnerable to aberrant early postnatal visual input. Yet, to date, how early experience might sculpt the temporal stability of human visual cortical processing has not been investigated. In CC individuals, we previously found a persistent and replicable reduction of the earliest event-related marker of extrastriate processing, the P1 wave. Here, we report that this robust reduction of the P1 in CC individuals results from an attenuated temporal coherence of cortical oscillations across trials, rather than from a generally reduced extrastriate cortical activation strength. In two experiments, compared to matched normally sighted controls, CC individuals (n = 12 and 13, respectively) exhibited diminished oscillatory phase coherence (i.e., higher temporal variability), rather than lower oscillatory amplitudes during visual processing. Furthermore, phase coherence information, but not activation strength, allowed classifying sight recovery individuals with congenital vs. developmental etiologies. Finally, exchanging the signal phase and activation strength information between CC and matched control individuals confirmed that group differences in P1 amplitude were largely driven by oscillatory timing. These group differences, specific to the CC group, were not found in groups of sight-recovery individuals who had suffered from developmental cataracts. Our results indicate that the intricate temporal orchestration of visual processing in human extrastriate cortex requires visual experience in an early postnatal sensitive period.