Disrupted developmental processes in the human visual cortex linked to congenital patterned visual deprivation

Abstract

Sensitive periods are maturational phases wherein the brain shows heighted plasticity in response to environmental experience. Importantly, if sensory experience was not received within such windows, development of the underlying neural architecture was found to be impaired. This dissertation investigated two hypothesized mechanisms underlying sensitive periods in the human visual cortex, by working with rare individuals who were born blind due to dense bilateral congenital cataracts. Due to delayed treatment, these individuals experienced a transient period of congenital patterned visual deprivation. The first two studies of this dissertation tested the role of two neural processes which, based on non-human animal research, were proposed to underlie sensitive periods of brain development. First, the maturation of inhibition in the visual cortex was shown to rely on visual experience in non-human animal models, resulting in the establishment of an E/I balance. To investigate whether the development of such an E/I balance in humans is linked to a sensitive period, the first study of this dissertation (Appendix I) compared the ratio of excitation to inhibition (E/I ratio) in the visual cortex of CC individuals to aged-matched normally sighted (SC) individuals. Magnetic Resonance Spectroscopy was used to compare the visual cortex concentrations of excitatory/inhibitory (Glutamate-glutamine/Gamma-Aminobutyric Acid) neurotransmitters. Additionally, the aperiodic parameters of the broadband (1-20 Hz) electroencephalogram (EEG) spectrum were compared across occipital electrodes. Previous work has linked the slope of the aperiodic EEG (1/f) distribution to the E/I ratio, whereas the intercept has been related to broadband neuronal firing. Both the neurotransmitter ratio and the aperiodic slope indicated a lower E/I ratio in the visual cortex of CC than SC individuals. Simultaneously, the aperiodic intercept was increased in CC individuals, suggesting increased broadband neuronal firing. These findings suggest that the development of human visual cortex E/I ratio might underlie sensitive period plasticity. Second, the development of corticocortical projections has been shown to rely on postnatal visual input in non-human animals. Corticocortical projections support the interaction between feedforward and feedback processing, i.e. recurrent processing, in the visual cortex, which is essential for typical visual behavior. Occipital alpha (8-14 Hz) oscillations have been correlated to feedback processing in SC individuals; therefore, the second study of this dissertation compared whether two characteristic EEG alpha-range phenomena manifest to the same extent in CC individuals (Appendix II). CC individuals demonstrated lower stimulus-evoked as well as resting-state alpha amplitudes than SC individuals. Further, CC individuals with above-threshold evoked alpha activity had better visual acuity than those without a significant evoked alpha peak. This linked reduction of evoked and resting- state alpha activity was interpreted as an impairment in recurrent processing in CC individuals’ visual systems. Together, these studies provide evidence for neural processes which demonstrate (visual) experience dependence, and therefore, might be associated with a sensitive period. In addition to deleterious effects on visual behavior, the consequences of congenital visual deprivation have been shown to extend to multisensory integration. The third study of this dissertation tested whether congenital visual deprivation affected the development of visuo-haptic integration by investigating whether CC individuals experience the Size-Weight illusion (SWI). The SWI is a robust illusion in typical visuo-haptic development, wherein SC individuals perceive the larger of two objects which in fact weigh the same to be lighter. In this study, CC and SC participants were first presented with visuo-haptic cues of size, i.e. being able to see and feel the objects. Additionally, individuals treated for developmental cataracts and permanently congenitally blind individuals were tested. All groups experienced a robust visuo-haptic SWI. Subsequently, CC participants assessed the weights of stimuli while receiving no haptic size information, i.e. holding them with an attached string. Regardless of whether size information was presented via visuo-haptic or exclusively visual cues, CC participants experienced the SWI to the same extent as SC individuals. These results suggested that the ability to integrate simultaneous visual and haptic size cues did not rely on early visual experience.