Mechanisms for Stable, Robust, and Adaptive Development of Orientation Maps in the Primary Visual Cortex

Abstract

Development of orientation maps in ferret and cat primary visual cortex (V1) has been shown to be stable, in that the earliest measurable maps are similar in form to the eventual adult map, robust, in that similar maps develop in both dark rearing and in a variety of normal visual environments, and yet adaptive, in that the final map pattern reflects the statistics of the specific visual environment. How can these three properties be reconciled? Using mechanistic models of the development of neural connectivity in V1, we show for the first time that realistic stable, robust, and adaptive map development can be achieved by including two low-level mechanisms originally motivated from single-neuron results. Specifically, contrast-gain control in the retinal ganglion cells and the lateral geniculate nucleus reduces variation in the presynaptic drive due to differences in input patterns, while homeostatic plasticity of V1 neuron excitability reduces the postsynaptic variability in firing rates. Together these two mechanisms, thought to be applicable across sensory systems in general, lead to biological maps that develop stably and robustly, yet adapt to the visual environment. The modeling results suggest that topographic map stability is a natural outcome of low-level processes of adaptation and normalization. The resulting model is more realistic, simpler, and far more robust, and is thus a good starting point for future studies of cortical map development.

Origins of the specialization for letters and numbers in ventral occipitotemporal cortex

“…Conversely, self-organizing models with shallow architectures have long been known to produce topographical and topological maps under a variety of activity-dependent learning rules [87][88][89][90][91][92]. One such model [90] simulates the emergence of separate areas for letters and digits by spontaneous symmetry-breaking, but fails to explain the systematic location of these cortical territories.…”

Functional implications of orientation maps in primary visual cortex

“…Later studies demonstrated that cortical orientation maps are organized in a mosaic consisting of iso-orientation domains arranged radially around pinwheel centres, where orientation preference changes rapidly along the circular locus234. Although many models have been proposed to explain how the beautiful geometrical properties of the pinwheel pattern could develop5678 and why they are remarkably similar across many species, the visual cortices of many mammals including rodents, squirrels and lagomorphs do not have orientation maps91011. Therefore, it remains a mystery whether topographically mapping stimulus orientation is an epi-phenomenon or has significant functional implications121314.…”

Neural plasticity and concepts ontogeny

“…This theoretical formulation has demonstrated the possibility of LTP and homeostasis in the formation of orientation, ocular dominance, and direction preferences in the primary visual cortex (Bednar and Miikkulainen 2006;Stevens et al 2013), the development of whisker direction maps in rat barrel cortex (Wilson et al 2010), and the formation of selectivity to angles in visual area V2 (Plebe 2007(Plebe , 2012.…”