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

Abstract

Numerous studies in visually deprived nonhuman animals have demonstrated sensitive periods for the functional development of the early visual cortex. However, in humans it is yet unknown which visual areas are shaped to which degree based on visual experience. The present study investigated the functional organization and processing capacities of early visual cortex in sight recovery individuals with either a history of congenital cataracts (CC) or late onset cataracts (developmental cataracts, DC). Visual event-related potentials (VERPs) were recorded to grating stimuli which were flashed in one of the four quadrants of the visual field. Participants had to detect rarely occurring grating orientations. The CC individuals showed the expected polarity reversal of the C1 wave between upper and lower visual field stimuli at the typical latency range. Since the C1 has been proposed to originate in the early retinotopic visual cortex, we concluded that one basic feature of the retinotopic organization, upper versus lower visual field organization, is spared in CC individuals. Group differences in the size and topography of the C1 effect, however, suggested a less precise functional tuning. The P1 wave, which has been associated with extrastriate visual cortex processing, was significantly attenuated in CC but not in DC individuals compared to typically sighted controls. The present study thus provides evidence for fundamental aspects of retinotopic processing in humans being independent of developmental vision. We suggest that visual impairments in sight recovery individuals may predominantly arise at higher cortical processing stages.

Sensory experience during early sensitive periods shapes cross-modal temporal biases

“…However, a previous study found longer switch times than in controls from audition to vision but not from vision to audition in CC-individuals whose cataracts had been removed in the first months of life, which was interpreted as indicating an attentional bias towards audition over vision 37 . Moreover, an attentional bias towards vision would have been expected to result in relatively shorter visual reaction times and early cortical potentials, which, as argued at the beginning of the Discussion is incompatible with the literature [33][34][35][36][37] . Thus, while scarce existing data points towards a reduced dominance perceptual judgments tend to rely more on prior information such as existing biases when the sensory information is uncertain 48,49 .…”

“…1F) indicated temporal processing impairments for vision but not for audition and touch. Consistently, studies measuring event-related potentials have provided no evidence for a shorter latency of the first visual cortical response in CC-individuals [33][34][35] and behavioral studies have demonstrated no advantage in reaction times to simple visual stimuli 36,37 . Moreover, reduced visual contrast -typical for cataract-reversal individuals -is associated with delayed responses of the visual system and lower visual temporal sensitivity 38,39 .…”

Successful visually guided eye movements following sight restoration after congenital cataracts

“…In fact, non-human animal studies have found a typical topography and typical receptive field sizes in the superior colliculus of visually deprived animals at the end of the deprivation period (King & Carlile, 1993;Vidyasagar, 1978). In accord with this finding a recent study found a retinotopic organization and typical latency of the first visual response (Sourav et al, 2018).…”

“…Individuals born with congenital, dense, total, bilateral cataracts provide a unique opportunity for research into the experience-dependent development of the human visual system as several of them do not receive patterned visual input until the cataracts are removed. Although some visual system functions appear to develop normally after sight is restored, such as color perception ( Brenner, Cornelissen, & Nuboer, 1990 ; McKyton, Ben-Zion, Doron, & Zohary, 2015 ; Pitchaimuthu, Sourav, Bottari, Banerjee, Shareef, Kekunnaya, & Röder, 2019 ), retinotopy ( Sourav, Bottari, Kekunnaya, & Röder, 2018 ), and biological motion detection ( Bottari, Troje, Ley, Hense, Kekunnaya, & Röder, 2015 ; Hadad, Maurer, & Lewis, 2012 ), others do not, leading to lasting impairments such as reduced visual acuity ( Ellemberg, Lewis, Maurer, Hong Lui, & Brent, 1999 ; Kalia et al, 2014 ), impaired face processing ( Le Grand, Mondloch, Maurer, & Brent, 2001 ; Putzar, Hötting, & Röder, 2010 ), reduced global motion perception ( Bottari, Kekunnaya, Hense, Troje, Sourav, & Röder, 2018 ; Hadad et al, 2012 ), and compromised multisensory speech perception ( Putzar, Hötting, Rösler, & Röder, 2007 ; Putzar et al, 2010 ). It could be hypothesized that these impairments stem from an impaired oculomotor control, preventing these individuals from systematically scanning the visual environment.…”

Cross-modal temporal biases emerge during early sensitive periods

“…However, CC-individuals' spatiotemporal resolution revealed a temporal processing impairment for vision but not for audition and touch. Consistently, event-related potentials have provided no evidence for earlier visuallyevoked brain activity in CC-individuals 10,11 and behavioral studies have demonstrated no visual advantage in reaction times to simple visual stimuli 12,13 . Moreover, reduced visual contrasttypical for cataract-reversal individuals -is associated with delayed responses of the visual system and lower visual temporal sensitivity 14,15 .…”