Abstract
In the primary visual cortex (V1) of higher mammals, long-range horizontal connections (LHCs) are observed to develop, linking iso-orientation domains of cortical tuning. It is unknown how this feature-specific wiring of circuitry develops before eye-opening. Here, we suggest that LHCs in V1 may originate from spatiotemporally structured feedforward activities generated from spontaneous retinal waves. Using model simulations based on the anatomy and observed activity patterns of the retina, we show that waves propagating in retinal mosaics can initialize the wiring of LHCs by coactivating neurons of similar tuning, whereas equivalent random activities cannot induce such organizations. Simulations showed that emerged LHCs can produce the patterned activities observed in V1, matching the topography of the underlying orientation map. The model can also reproduce feature-specific microcircuits in the salt-and-pepper organizations found in rodents. Our results imply that early peripheral activities contribute significantly to cortical development of functional circuits.SIGNIFICANCE STATEMENT Long-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, thereby selectively connecting iso-domains of orientation map. However, it is unknown how such feature-specific wirings develop before eye-opening. Here, we show that LHCs in V1 may originate from the feature-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings in the V1 neurons. Our model also explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is universally applicable to circuits of various mammalian species.
Highlights
In the primary visual cortex (V1) of higher mammals, neurons are observed to respond selectively to the orientations of visual stimuli, and their preferred orientations are organized into columnar orientation maps (Blasdel and Salama, 1986) (Fig. 1A)
From the model simulations of early visual pathways, we show that spontaneous retinal activity before eye-opening, which is spatiotemporally constrained by retinal mosaics circuitry, may selectively activate V1 neurons of similar orientation tuning and lead to development of Long-range horizontal connections (LHCs) via activity-dependent cortical plasticity
Based on the experimental observation that inhibitory transduction of amacrine cells (ACs) induces temporal delay between the bursting activity of ON and OFF RGCs (Akrouh and Kerschensteiner, 2013; Firl et al, 2015), our retinal wave model (Fig. 3B) simulates spontaneous activity as follows: an ON wavefront is formed by local excitatory networks of ON RGCs
Summary
Long-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, thereby selectively connecting iso-domains of orientation map. It is unknown how such feature-specific wirings develop before eye-opening. We show that LHCs in V1 may originate from the feature-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings in the V1 neurons. Our model explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is universally applicable to circuits of various mammalian species
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