Refinement but Not Maintenance of Visual Receptive Fields Is Independent of Visual Experience

Abstract

Visual deprivation is reported to prevent or delay the development of mature receptive field (RF) properties in primary visual cortex (V1) in several species. In contrast, visual deprivation neither prevents nor delays refinement of RF size in the superior colliculus (SC) of Syrian hamsters, although vision is required for RF maintenance in the SC. Here, we report that, contrary to expectation, visual cortical RF refinement occurs normally in dark-reared animals. As in the SC, a brief period of visual experience is required to maintain V1 RF refinement in adulthood. Whereas in the SC, 3 days of visual experience within a sensitive period (P37-40) was sufficient to protect RFs from deprivation-induced enlargement in adulthood, 7 days (P33-40) were required for RF size maintenance in V1. Thus, spontaneous activity is sufficient for RF refinement at these 2 levels of the visual pathway, and visual input is necessary only to prevent deprivation-induced RF enlargement in adulthood. These studies show that sensory experience during a late juvenile sensitive period protects the visual pathway against sensory deprivation in adulthood, and suggest that more importance may have been placed on the role of early visual experience in visual RF development than is warranted.

TrkB Activation During a Critical Period Mimics the Protective Effects of Early Visual Experience on Perception and the Stability of Receptive Fields in Adult Superior Colliculus

“…The visual stimulus consisted of a bright white square traveling from dorsal to ventral visual field at 14°/s across a black background. The stimulus size was 1 degree in diameter and each vertical traverse shifted 2° along the x axis of the monitor after each presentation, with a 3 second inter-stimulus interval, as in (Balmer and Pallas, 2015a).…”

“…Chronic dark rearing (DR) beyond postnatal day (P) 60 results in expansion of RFs to juvenile size (Carrasco et al, 2005). Light exposure during an early postnatal critical period protects RFs against this later loss of refinement (Carrasco and Pallas, 2006;Balmer and Pallas, 2015a). Thus, in contrast to RF refinement in cats and primates (see Shatz, 1996, for review), development of refined RFs in hamster SC and V1 is independent of sensory experience, and requires vision only for maintenance.…”

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During a critical period in development, spontaneous and evoked retinal activity shape visual pathways in an adaptive fashion. Interestingly, spontaneous activity is sufficient for spatial refinement of visual receptive fields in superior colliculus (SC) and visual cortex (V1), but early visual experience is necessary to maintain inhibitory synapses and stabilize RFs in adulthood (Carrasco et al 2005(Carrasco et al , 2011Carrasco & Pallas 2006;Balmer & Pallas 2015a). In visual cortex (V1), brain-derived neurotrophic factor (BDNF) and its high affinity receptor TrkB are important for development of visual acuity, inhibition, and regulation of the critical period for ocular dominance plasticity (Hanover et al, 1999;Huang et al, 1999;Gianfranceschi et al, 2003).

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The case from animal studies for balanced binocular treatment strategies for human amblyopia

“…As examples of the first scenario, cells in the ferret visual cortex do not develop directional selectivity at all in the absence of visual experience while ocular dominance maps in the mouse visual cortex are subject to experiential modification from about the time of eye‐opening . In contrast, the receptive field dimensions of cells in the visual cortex of Syrian hamsters mature normally in the absence of any visual input and visual experience appears necessary only to prevent degradation of receptive field properties if animals remain in darkness into adulthood …”

“…61 In contrast, the receptive field dimensions of cells in the visual cortex of Syrian hamsters mature normally in the absence of any visual input and visual experience appears necessary only to prevent degradation of receptive field properties if animals remain in darkness into adulthood. 62 In higher mammals the second experience-dependent stage of development begins at a time when the organization of the visual pathways has been largely established through programs of gene action, so that visually-driven activity acts upon a pre-existing scaffold. As a consequence, certain visual stimuli that are matched closely to the preexisting functional scaffold may provide a more effective excitatory drive and hence exert a greater effect on subsequent development than other stimuli.…”