Typical resting-state activity of the brain requires visual input during an early sensitive period

Abstract

Sensory deprivation, following a total loss of one sensory modality e.g. vision, has been demonstrated to result in compensatory plasticity. It is yet not known to which extent neural changes, e.g. higher resting state activity in visual areas (cross-modal plasticity) as a consequence of blindness, reverse, when sight is restored. Here, we used functional MRI to acquire blood oxygen level dependent (BOLD) resting state activity during an eyes open (EO) and an eyes closed (EC) state in congenital cataract-reversal individuals, developmental cataract-reversal individuals, congenitally permanently blind individuals and sighted controls. The amplitude of low frequency fluctuations (ALFF) of the BOLD signal - a neural marker of spontaneous brain activity during rest - was analyzed. In accord with previous reports, in normally sighted controls we observed an increase in ALFF during rest with the EO compared to rest with EC in visual association areas and in parietal cortex but a decrease in auditory and sensorimotor regions. In congenital cataract-reversal individuals, we found an increase of the amplitude of slow BOLD fluctuations in visual cortex during rest with EO compared to rest with EC too but this increase was larger in amplitude than in normally sighted controls. In contrast, congenital cataract-reversal individuals lagged a similar increase in parietal regions and did not show the typical decrease of ALFF in auditory cortex. Congenitally blind individuals displayed an overall higher amplitude in slow BOLD fluctuations in visual cortex compared to sighted individuals and compared to congenital cataract-reversal individuals in the EC condition. Higher ALFF in visual cortex of congenital cataract-reversal individuals than in normally sighted controls during EO might indicate an altered excitatory-inhibitory balance of visual neural circuits. By contrast, the lower parietal increase and the missing downregulation in auditory regions suggest a reduced influence of the visual system on multisensory and the other sensory systems after restoring sight in congenitally blind individuals. These results demonstrate a crucial dependence of visual and multisensory neural system functioning on visual experience during a sensitive phase in human brain development.

Neural correlates of theory of mind reasoning in congenitally blind children

“…3 ). These differences are difficult to interpret, though consistent with evidence that the magnitude of activation (often estimated via the amplitude of activity in the low frequency range of the BOLD response) in several brain regions, including precuneus and parietal cortex, varies in adults depending on whether their eyes are open or closed (e.g., Rączy et al, 2022 ). One possibility is that these differences are secondary consequences of previously observed differences in response magnitude in lower-level visual brain regions, including the fusiform gyrus, in these same children ( Bedny et al, 2015 ).…”

Altered visual cortex excitatory/inhibitory ratio following transient congenital visual deprivation in humans

“…Further, neuronal spiking was increased in dark reared mice when exposed to ambient light (Benevento et al, 1992). Crucially, increased visual cortex thickness (Feng et al, 2021; Guerreiro et al, 2015; Hölig et al, 2023) and higher BOLD activity during rest with the eyes open (Raczy et al, 2022) have been observed for CC individuals as well, suggesting incomplete recovery of cortical structure and function after sight restoration in humans. Thus, the restored feedforward drive to visual cortex after surgery might reach a visual cortex with a lower threshold for excitation, possible due to a relatively higher number of excitatory synapses (Bourgeois, 1996; Morales et al, 2002).…”

“…These visual deficits in congenital cataract-reversal individuals have been attributed to altered neural development due to the absence of vision, as individuals who suffered from developmental cataracts do not typically display a comparable severity of impairments (Lewis & Maurer, 2009; Sourav et al, 2020). While extant literature reported correlations between structural changes and behavioral outcomes in congenital cataract-reversal individuals (Feng et al, 2021; Guerreiro et al, 2015; Hölig et al, 2023; Pedersini et al, 2023), functional brain imaging (Heitmann et al, 2023; Raczy et al, 2022) and electrophysiological research (Bottari et al, 2016; Ossandón et al, 2023; Pant et al, 2023; Pitchaimuthu et al, 2021) have started to unravel the neural mechanisms which rely on visual experience during sensitive periods for development.…”

“…Resting-state activity measured via fMRI suggested an increased E/I ratio in the visual cortex of congenital cataract-reversal individuals (Raczy et al, 2022): The amplitude of low frequency (<1 Hz) (blood oxygen level-dependent) fluctuations (ALFF) in visual cortex was increased in congenital cataract-reversal individuals compared to normally-sighted controls when they were scanned with their eyes open. Since similar changes were observed in permanently congenitally blind humans, the authors speculated that congenital visual deprivation resulted in increased E/I ratio of neural circuits due to impaired neural tuning, which was not reinstated after sight restoration (Raczy et al, 2022). Other studies measured resting-state electroencephalogram (EEG) activity and analyzed periodic (alpha oscillations) (Bottari et al, 2016; Ossandón et al, 2023; Pant et al, 2023) as well as aperiodic activity (Ossandón et al, 2023).…”