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David Whitney, Gordon Smith, Bettina Hein, Matthias Kaschube, David Fitzpatrick; High cellular and columnar variability underlies the absence of early orientation selectivity. Journal of Vision 2017;17(10):1107. doi: https://doi.org/10.1167/17.10.1107.
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© ARVO (1962-2015); The Authors (2016-present)
Selectivity for stimulus orientation is a fundamental property of primary visual cortex in primates and carnivores, where it is organized into a smoothly varying columnar map that emerges in an activity-dependent manner during early postnatal life. Despite extensive experimental and theoretical work, it remains unclear what factors limit the emergence of orientation selectivity, such as weak responsiveness to visual stimuli, high trial-to-trial variability, and/or an intermixed 'salt-and-pepper' organization of orientation preferences at the cellular level. To distinguish between these potential factors, we visualized population activity in the visual cortex of developing ferrets with longitudinal imaging of GCAMP6s at both cellular resolution with two-photon calcium imaging and columnar resolution with wide-field epifluorescence imaging. Prior to eye opening, we show that cellular and population responses evoked by single presentations of a grating stimulus surprisingly exhibit robust, modular patterns of network activity resembling activity patterns evoked by gratings in mature animals. However, the spatial location and pattern of domains activated by presentation of the identical stimulus orientation varies substantially across trials, a variability that accounts for the low orientation selectivity of individual neurons and the inability to visualize coherent maps of orientation preference. Yet variability in network activity patterns is not a general feature of the developing cortex, as the modular patterns of network activity evoked by uniform luminance steps are already selective at these ages. Furthermore, we show that trial-averaged activity patterns evoked by gratings show similarity to the mature orientation map as early as 1-2 days prior to eye opening. We conclude that the early disassociation between stimulus orientation and consistent patterns of modular network activity is a major factor underlying the absence of orientation selectivity in a developing cortical network already exhibiting highly modular functional organization.
Meeting abstract presented at VSS 2017
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