Recurrent circuits encode visual center-surround computations in the mouse superior colliculus
Authors:
- Peng CuiPCPeng Cui
- Kuisong SongKSKuisong Song
- Dimitris Mariatos-MetaxasDMDimitris Mariatos-Metaxas
- Arturo G. IslaAIArturo G. Isla
- Teresa FemeniaTFTeresa Femenia
- Iakovos LazaridisILIakovos Lazaridis
- Konstantinos MeletisKMKonstantinos Meletis
- Arvind KumarAKArvind Kumar
- Andreas A. KardamakisAKAndreas A. Kardamakis
Preprint
Abstract
Center-surround interactions are fundamental to visual saliency computation, but debate continues over whether and how subcortical visual circuits actively contribute. To address this, we developed an optogenetic approach to delineate the visual center and surround zones of individual neurons in the superficial layer of the superior colliculus (SCs) using only retinal ganglion cell input. Using whole-cell recordings, we demonstrate that surround network activation suppresses center excitability, indicating that SCs circuitry is self-sufficient in driving center-surround dynamics. Through cell-type-specific trans-synaptic tracing and large-scale modeling, we identified an SCs-based circuit with two key motifs driving surround modulation: recurrent excitation and feedback inhibition. We propose that subcortical visual circuits in the SCs have evolved to perform surround suppression alongside retinal and cortical suppression, facilitating the distribution of parallel saliency computations across different levels. Significance statement: This study questions the notion that the superior colliculus (SC) merely acts as a passive recipient of saliency information from upstream circuits. We demonstrate that the SC can independently generate center-surround interactions that could contribute to visual saliency through local circuits without top-down input. This ability represents a computation that has been conserved since the dawn of vertebrate evolution. By mapping these interactions, we reveal that the mouse SC actively induces visual surround suppression. These findings suggest that phylogenetically older circuits in the SC may play a more independent role in active vision than previously acknowledged, prompting a reevaluation of visual saliency processing across subcortical brain regions.Keywords
All Related Versions
This publication has 45 references indexed in Scilit:
- The most numerous ganglion cell type of the mouse retina is a selective feature detectorProceedings of the National Academy of Sciences, 2012
- Surround suppression and sparse coding in visual and barrel corticesFrontiers in Neural Circuits, 2012
- Lateral presynaptic inhibition mediates gain control in an olfactory circuitNature, 2008
- Suppressive Surrounds and Contrast Gain in Magnocellular-Pathway Retinal Ganglion Cells of MacaqueJournal of Neuroscience, 2006
- The Suppressive Field of Neurons in Lateral Geniculate NucleusJournal of Neuroscience, 2005
- MOLECULAR GRADIENTS AND DEVELOPMENT OF RETINOTOPIC MAPSAnnual Review of Neuroscience, 2005
- Deficits in saccade target selection after inactivation of superior colliculusNature Neuroscience, 2004
- Neural Representation and Neural ComputationPhilosophical Perspectives, 1990
- The quantized geometry of visual space: The coherent computation of depth, form, and lightnessBehavioral and Brain Sciences, 1983
- Center-Surround Organization of Auditory Receptive Fields in the OwlScience, 1978