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Authors & Affiliations
Kai Lun Teh,Jeremie Sibille,Jens Kremkow
Abstract
The upper visual layers of the mouse superior colliculus (SC) exhibit an orientation preference map (OPM) with a retinotopy-based concentric pattern (Ahmadlou and Heimel, 2015; Feinberg and Meister, 2015; but see Chen et al., 2020). The underlying developmental mechanisms that give rise to this concentric OPM in the mouse SC are still unclear. During visual system development, the stage III (S3) retinal waves are known to play important roles in circuit formation. Specifically, the S3 waves that tend to propagate towards the caudal direction (Gribizis et al., 2019) have impacts on the direction selectivity of the SC neurons (Ge et al., 2021). In addition, the OFF retinal ganglion cells (RGCs) are recruited with a time-delay relative to ON RGCs during S3 waves (Kerschensteiner and Wong, 2008). Here, we propose that these S3 wave directionality biases, together with the OFF-ON delay, play an instructive role in establishing the OPM during development. To test this hypothesis, we built a model that incorporates the above-mentioned S3 wave features to predict the properties of the established OPM. The Hebbian mechanism was used to refine the RGC-SC connections during S3 waves to show that the OFF delays can segregate the ON- and OFF-RGC connections to individual SC neurons, which locally give rise to the orientation preference. Furthermore, we show that the biases in S3 wave directionality can mediate the formation of a concentric OPM. In summary, our model suggests that OFF delay of S3 waves can mediate local microscopic segregation of the ON-OFF subfields of the postsynaptic SC neurons, whereas the biases in the wave propagating direction determine the overall macroscopic organization of the OPM. Taken together, these findings suggest that the S3 waves could instruct the formation of the OPM in the mouse SC by fine-tuning the receptive fields of the postsynaptic SC neurons.