Recurrent circuits encode visual center-surround computations in the mouse superior colliculus

Abstract

Extraretinal circuits can shape visual center-surround interactions that originate in the retina, yet the contributing circuit mechanisms to this initial modulation remain elusive. Using an optogenetic-based approach applied to the superficial layers of the superior colliculus (SCs), we demonstrate that the SCs is sufficient in generating surround suppression through selective patterned activation of visual center and surround zones in individual neurons. Like in the primary visual cortex, surround network activation causes decreases in center excitation rather than increases in synaptic inhibition. We reveal the identity of a SCs-based circuit with two interacting circuit motifs, recurrent excitation and feedback inhibition, capable of modulating levels of center excitation when the visual surround is active, using whole-cell recordings, trans-synaptic mapping, and functional approaches with computational modeling. We propose that early subcortical and cortical visual circuits have evolved to perform surround modulation independently, thereby enhancing visuospatial versatility across multiple levels.