Lateralized Visuotopic Organization of the Macaque Superior Colliculus

Abstract

The superior colliculus (SC) integrates multisensory inputs from retinal, subcortical, and cortical regions within a map of visual space to support orienting and interactive behaviors. While early models suggested that the SC primarily represents extrafoveal space for target detection, recent evidence highlights its significant foveal representation, essential for precisely targeting objects. Using ultra-high-resolution phase-encoding fMRI and spatially localized stimuli, we mapped the visuotopic organization of the SC in six macaques up to 40° eccentricity. In addition to confirming previous findings, we identified a non-retinotopic, context-dependent foveal representation and robust interhemispheric functional asymmetries. The left SC emphasizes central vision and eccentricity information, whereas the right SC primarily encodes peripheral and polar angle information. Whole-brain analyses revealed that only the intraparietal sulcus, a major cortical input to the SC, exhibited similar lateralized patterns. These findings suggest that functional lateralization in nonhuman primates is more prevalent than previously recognized, with left-dominant targeting and right-dominant spatial monitoring. This aligns with patterns observed across species with lateralized brains, including humans.

Note:
Funding declaration: This work was funded by the European Research Council (ERC LightUp under grant agreement 772953) and from the sub-project (bando a cascata) “SPARKS” (CUP D93C22000930002) to M.T.; received internal funds of the KU Leuven C14/21/111, IDN/20/016, C3/21/027; Fonds Wetenschappelijk Onderzoek-Vlaanderen (FWO-Flanders) G0E0520N, G0C1920N to W.V.; PRIN 2022 (Grant ID: 2022NEE53Z) from the Ministry of University and Research (MUR); the National Recovery and Resilience Plan (PNRR) and #NEXTGENERATIONEU (NGEU) project “MNESYS” (PE00000006) – A Multiscale integrated approach to the study of the nervous system in health and disease (DN. 1553 11.10.2022) to L.B..

Conflict of Interests: The authors declare no competing interest.

Ethical Approval: Animal care and experimental procedures followed national and European regulations (Directive 2010/63/EU) and were approved by the Ethical Committee of KU Leuven.

Keywords: superior colliculus, intraparietal sulcus, high-resolution fMRI, lateralization, interhemispheric functional asymmetry, nonhuman primates, retinotopy