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Authors & Affiliations
Alexandra Gribizis, David Fitzpatrick
Abstract
A characteristic feature of developing sensory circuits is spontaneous co-activations that initiate organized networks and maps in preparation for sensory experience. In species such as primates and carnivores, the mature visual cortex is characterized by iterated clusters of similarly responding neurons, or modules, and provides an excellent model system for exploring the mechanisms underlying the development of functional network organization. The sequence of early events that leads to the initial emergence of modular network structure remains unknown. Interestingly during this period of early visual system development, linear wavefronts of spontaneous activity also sweep across the retina and downstream visual pathways before eye opening in many species. Here we employ chronic calcium imaging in tree shrew visual cortex starting a week before eye opening to examine the contribution of patterned spontaneous feed-forward activity for setting up mature cortical networks.
We find that patterned spontaneous waves are broad and unspecific early in the developing visual cortex and then rapidly transform within a day into a modular coactivation of multiple patches extending millimeters across the cortical surface. Surprisingly, early on, we find a correlation between wavefront trajectory and modular pattern identity, with orthogonal wavefronts activating complimentary modular patterns. These wavefronts create an axial bias in spontaneous modular pattern associations, resembling mature horizontal connectivity (Bosking et al. 1997) before sensory experience, an anisotropy that diminishes after cholinergic blockade of wave activity. Finally, we find that the axis of correlation patterns in spontaneous activity is predictive of future orientation responses, strengthening in their resemblance to evoked patterns up to and through eye opening. Our results provide the first experimental evidence for the relationship between slowly propagating waves in visual cortex and the formation of orientation columns, demonstrating that waves precede modular network formation and provide a simulated axial alignment for mature functional networks.