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

Abstract The interaction of retinal center-surround processes with early visual subcortical and cortical circuits forms the basis for saliency computations. The subcortical circuit mechanisms contributing to surround modulation, however, remain unclear. We developed an optogenetic approach to functionally delineate visual center and surround zones of individual neurons in the superficial layers of the superior colliculus (SCs). We demonstrate that local circuit interactions within the SCs are sufficient to generate visual surround suppression. Notably, surround network activation leads to decreases in center excitation rather than increases in synaptic inhibition. Using a range of complementary methods, we reveal the identity of a SCs-based circuit with two key interacting circuit motifs, recurrent excitation and feedback inhibition, capable of modulating levels of center excitation when the visual surround is active. We propose that subcortical and cortical visual circuits are both recurrent-based and have evolved to independently perform surround modulation, thus enabling parallel saliency computations across multiple levels.