Novel Models of Visual Topographic Map Alignment in the Superior Colliculus

The establishment of precise neuronal connectivity during development is critical for sensing the external environment and informing appropriate behavioral responses. In the visual system, many connections are organized topographically, which preserves the spatial order of the visual scene. The superior colliculus (SC) is a midbrain nucleus that integrates visual inputs from the retina and primary visual cortex (V1) to regulate goal-directed eye movements. In the SC, topographically organized inputs from the retina and V1 must be aligned to facilitate integration. Previously, we showed that retinal input instructs the alignment of V1 inputs in the SC in a manner dependent on spontaneous neuronal activity; however, the mechanism of activity-dependent instruction remains unclear. To begin to address this gap, we developed two novel computational models of visual map alignment in the SC that incorporate distinct activity-dependent components. First, a Correlational Model assumes that V1 inputs achieve alignment with established retinal inputs through simple correlative firing mechanisms. A second Integrational Model assumes that V1 inputs contribute to the firing of SC neurons during alignment. Both models accurately replicate in vivo findings in wild type, transgenic and combination mutant mouse models, suggesting either activity-dependent mechanism is plausible. In silico experiments reveal distinct behaviors in response to weakening retinal drive, providing insight into the nature of the system governing map alignment depending on the activity-dependent strategy utilized. Overall, we describe novel computational frameworks of visual map alignment that accurately model many aspects of the in vivo process and propose experiments to test them.
Author Summary In order to process sensory stimuli, precise connections must be established between sensory neurons during development. In the visual system, many connections are organized topographically, such that neighboring neurons monitor adjacent regions of space. In the superior colliculus (SC), converging topographic inputs must be aligned with one another to facilitate integration and preserve the spatial order of the visual scene. In this paper, we propose two novel computational models to describe the alignment of visual inputs in the SC. We demonstrate that both models are able to replicate experimental data obtained from wild type and mutant animals. Interestingly, each model performed differently in response to hypothetical experiments, suggesting they could be differentiated empirically. Thus, we put forth testable models of visual map alignment in the SC and propose experiments to determine which may be used during development.