Revisiting horizontal connectivity rules in V1: from like-to-like towards like-to-all

Abstract

Horizontal connections in the primary visual cortex of carnivores, ungulates and primates organize on a near-regular lattice. Given the similar length scale for the regularity found in cortical orientation maps, the currently accepted theoretical standpoint is that these maps are underpinned by a like-to-like connectivity rule: horizontal axons connect preferentially to neurons with similar preferred orientation. However, there is reason to doubt the rule's explanatory power, since a growing number of quantitative studies show that the like-to-like connectivity preference and bias mostly observed at short-range scale, are highly variable on a neuron-to-neuron level and depend on the origin of the presynaptic neuron. Despite the wide availability of published data, the accepted model of visual processing has never been revised. Here, we review three lines of independent evidence supporting a much-needed revision of the like-to-like connectivity rule, ranging from anatomy to population functional measures, computational models and to theoretical approaches. We advocate an alternative, distance-dependent connectivity rule that is consistent with new structural and functional evidence: from like-to-like bias at short horizontal distance to like-to-all at long horizontal distance. This generic rule accounts for the observed high heterogeneity in interactions between the orientation and retinotopic domains, that we argue is necessary to process non-trivial stimuli in a task-dependent manner.

Keywords: Computational and theoretical neuroscience; Connectivity rules; Functional optical imaging; Horizontal intra-cortical axons; Orientation and retinotopic maps; Primary visual cortex; Structural advanced anatomy.