Abstract
Sensory processing requires proper alignment of neural maps throughout the brain. In the superficial layers of the superior colliculus of the midbrain, converging projections from retinal ganglion cells and neurons in visual cortex must be aligned to form a visuotopic map, but the basic mechanisms mediating this alignment remain elusive. In a new mouse model, ectopic expression of ephrin-A3 (Efna3) in a subset of retinal ganglion cells, quantitatively altering the retinal EFNAs gradient, disrupts cortico-collicular map alignment onto the retino-collicular map, creating a visuotopic mismatch. Genetic inactivation of ectopic EFNA3 restores a wild-type cortico-collicular map. Theoretical analyses using a new mapping algorithm model both map formation and alignment, and recapitulate our experimental observations. The algorithm is based on an initial sensory map, the retino-collicular map, which carries intrinsic topographic information, the retinal EFNAs, to the superior colliculus. These EFNAs subsequently topographically align ingrowing visual cortical axons to the retino-collicular map.
Highlights
Brain function relies on the efficient processing of sensory information, which in turn requires the proper formation and interaction of multiple sensory maps of the world
These data confirm a two-fold ectopic expression of Efna3 in Isl2(+) Efna3KI/KI RGCs, which generates an oscillating high-nasal to low-temporal gradient in Efnas expression in the Efna3 KI mouse, very similar to the oscillating Ephas gradient we previously described for Isl2-Epha3 knock-in mice (Reber et al, 2004)
We describe a molecular mechanism and associated principles governing the alignment of converging topographic neural maps in the brain
Summary
Brain function relies on the efficient processing of sensory information, which in turn requires the proper formation and interaction of multiple sensory maps of the world. Visual information reaches the superficial layers of the SC, which are innervated both by retinal ganglion cells (RGCs - the retino-collicular projection) and by layer V neurons of the primary visual cortex V1 (the cortico-collicular projection). During development in the mouse, the retino-collicular map forms during the first post-natal week, and is followed by the cortico-collicular map, which develops between P6 and P12 (Triplett et al, 2009). These visuotopic maps must be aligned to ensure efficient modulation of the SC’s retinal response by V1 inputs (Zhao et al, 2014; Liang et al, 2015).
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