Sight restoration after congenital blindness does not reinstate alpha oscillatory activity in humans

Abstract

Functional brain development is characterized by sensitive periods during which experience must be available to allow for the full development of neural circuits and associated behavior. Yet, only few neural markers of sensitive period plasticity in humans are known. Here we employed electroencephalographic recordings in a unique sample of twelve humans who had been blind from birth and regained sight through cataract surgery between four months and 16 years of age. Two additional control groups were tested: a group of visually impaired individuals without a history of total congenital blindness and a group of typically sighted individuals. The EEG was recorded while participants performed a visual discrimination task involving intact and scrambled biological motion stimuli. Posterior alpha and theta oscillations were evaluated. The three groups showed indistinguishable behavioral performance and in all groups evoked theta activity varied with biological motion processing. By contrast, alpha oscillatory activity was significantly reduced only in individuals with a history of congenital cataracts. These data document on the one hand brain mechanisms of functional recovery (related to theta oscillations) and on the other hand, for the first time, a sensitive period for the development of alpha oscillatory activity in humans.

Induced cortical responses require developmental sensory experience

“…In the ongoing activity we observed a reduced alpha power in PAF of CDCs corresponding to the findings in the visual system of subjects with neonatal cataracts ( Bottari et al , 2016 ). The present study extends the previous result by demonstrating that the effect is also observed in the auditory domain and that it can be localized to a higher-order sensory area.…”

Evidence of a retinotopic organization of early visual cortex but impaired extrastriate processing in sight recovery individuals

“…The P1 wave has been hypothesized to be functionally closely related to alpha oscillations by Freunberger et al (2008), who suggested that both alpha activity and the P1 wave might reflect activity connected to the inhibition of neural systems related to ''task-irrelevant brain areas or task-irrelevant stimulus categories'' (p. 2339). As discussed above, Bottari et al (2016Bottari et al ( , 2018 found evidence that alpha oscillatory activity is compromised in CC individuals, suggesting that the neural mechanisms regulating the excitatory-inhibitory balance might be compromised as a result of congenital visual deprivation. Such an imbalance might manifest itself not only as alpha oscillatory deficits, but additionally might underlie the generally reduced P1 amplitude.…”

“…On the one hand, a lack of pruning might spread the visual stimulus driven activity to a larger number of neurons contralateral to the visual field in which the stimuli were presented. On the other hand, Bottari et al (2016) reported that alpha oscillatory activity was significantly reduced in CC individuals compared to MC and DC individuals. Alpha activity has often been associated with the regulation of the excitatory/inhibitory balance of neural circuits and has been linked to inhibitory neural circuit activity (Jensen & Mazaheri, 2010).…”

Biological Action Identification Does Not Require Early Visual Input for Development

“…In the context of indistinguishable CM thresholds in the SC and VM group, the present results suggest that the CM processing deficits of the CC individuals must be because of changes in the neural circuits associated with CM processing. In fact, a previous EEG study reported that α oscillations which have been associated with global motion processing ( Händel et al, 2007 ) were greatly reduced in CC individuals ( Bottari et al, 2016 ). It could be argued that the selective deficit in CM perception of CC individuals was predominantly because of the presence of nystagmus in this group.…”

“…In humans, studies in individuals treated for congenital cataracts (CC) have revealed incomplete recovery in many visual functions, including visual acuity (VA; Ellemberg et al, 1999 ), stereovision ( Tytla et al, 1993 ), visual feature binding ( Putzar et al, 2007 ; McKyton et al, 2015 ), global motion processing ( Ellemberg et al, 2002 ; Bottari et al, 2018 ), and face processing ( Le Grand et al, 2001 ; Röder et al, 2013 ), while functions such as color discrimination ( Brenner et al, 1990 ; Pitchaimuthu et al, 2019 ) seemed to emerge independently of early visual experience. Biological motion (BM) processing, e.g., the ability to detect the movement of biological figures with sparse information ( Johansson, 1973 ), has been shown to recover well following early visual deprivation ( Hadad et al, 2012 ), that is, both detection thresholds as well as neural signatures have been observed to be indistinguishable between a CC group and normally sighted controls (SC group; Bottari et al, 2015 , 2016 ).…”