Abstract
The superior colliculus (SC) receives diverse and robust cortical inputs to drive a range of cognitive and sensorimotor behaviors. However, it remains unclear how descending cortical input arising from higher-order associative areas coordinate with SC sensorimotor networks to influence its outputs. Here, we construct a comprehensive map of all cortico-tectal projections and identify four collicular zones with differential cortical inputs: medial (SC.m), centromedial (SC.cm), centrolateral (SC.cl) and lateral (SC.l). Further, we delineate the distinctive brain-wide input/output organization of each collicular zone, assemble multiple parallel cortico-tecto-thalamic subnetworks, and identify the somatotopic map in the SC that displays distinguishable spatial properties from the somatotopic maps in the neocortex and basal ganglia. Finally, we characterize interactions between those cortico-tecto-thalamic and cortico-basal ganglia-thalamic subnetworks. This study provides a structural basis for understanding how SC is involved in integrating different sensory modalities, translating sensory information to motor command, and coordinating different actions in goal-directed behaviors.
Highlights
The superior colliculus (SC) receives diverse and robust cortical inputs to drive a range of cognitive and sensorimotor behaviors
Single anterograde tracer injections of either Phaseolus vulgaris leucoagglutinin (PHAL), or adeno-associated viruses expressing green (AAV-GFP), or red (AAV-tdTomato) fluorescent protein were confined to a single cortical area to produce regional specific projection terminal patterns in the SC
We carried out double or triple tracer injections with combinations of PHAL, AAVs encoding enhanced green fluorescent protein (AAV-GFP), and AAV-tdTomato to determine direct spatial correlations of axonal terminals arising from different cortical areas
Summary
The superior colliculus (SC) receives diverse and robust cortical inputs to drive a range of cognitive and sensorimotor behaviors. Combining state-of-the-art circuit mapping and viral tracing methods with computational neuroanatomical tools, we assembled the first detailed connectivity map of descending cortical subnetworks to the SC, the cortico-tectal projectome, and concurrently constructed a brain-wide wiring diagram for the SC. This comprehensive resource provides a foundational structural model for the mouse SC that supports working hypotheses of regionally defined functions (such as flight vs freezing or approach vs aggression), and network- and cell-type-specific functions. These four subnetworks of the SC provide a structural basis for understanding different functional roles of the SC in coordinating movements of eyes, head and neck, whisker, mouth, and limbs in goal-oriented tasks such as attentive orientation, spatial navigation, and exploratory (i.e., prey capture), appetitive/approach, consummatory (i.e., chewing, swallowing, and biting) behaviors
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