The development of oscillatory and aperiodic resting state activity is linked to a sensitive period in humans

•Permanent and transient congenital blindness reduces alpha EEG activity.•Permanent and transient congenital blindness increases gamma EEG activity.•These results and an altered aperiodic activity suggest an increased E/I balance.•The EEG resting state profile depends on experience during a sensitive period. Congenital blindness leads to profound changes in electroencephalographic (EEG) resting state activity. A well-known consequence of congenital blindness in humans is the reduction of alpha activity which seems to go together with increased gamma activity during rest. These results have been interpreted as indicating a higher excitatory/inhibitory (E/I) ratio in visual cortex compared to normally sighted controls. Yet it is unknown whether the spectral profile of EEG during rest would recover if sight were restored. To test this question, the present study evaluated periodic and aperiodic components of the EEG resting state power spectrum. Previous research has linked the aperiodic components, which exhibit a power-law distribution and are operationalized as a linear fit of the spectrum in log-log space, to cortical E/I ratio. Moreover, by correcting for the aperiodic components from the power spectrum, a more valid estimate of the periodic activity is possible. Here we analyzed resting state EEG activity from two studies involving (1) 27 permanently congenitally blind adults (CB) and 27 age-matched normally sighted controls (MCB); (2) 38 individuals with reversed blindness due to bilateral, dense, congenital cataracts (CC) and 77 age-matched sighted controls (MCC). Based on a data driven approach, aperiodic components of the spectra were extracted for the low frequency (Lf-Slope 1.5 to 19.5 Hz) and high frequency (Hf-Slope 20 to 45 Hz) range. The Lf-Slope of the aperiodic component was significantly steeper (more negative slope), and the Hf-Slope of the aperiodic component was significantly flatter (less negative slope) in CB and CC participants compared to the typically sighted controls. Alpha power was significantly reduced, and gamma power was higher in the CB and the CC groups. These results suggest a sensitive period for the typical development of the spectral profile during rest and thus likely an irreversible change in the E/I ratio in visual cortex due to congenital blindness. We speculate that these changes are a consequence of impaired inhibitory circuits and imbalanced feedforward and feedback processing in early visual areas of individuals