Organization of the inputs and outputs of the mouse superior colliculus

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.

Functional Organisation of the Mouse Superior Colliculus

“…Neurons in the 'motor-related' parts of SC can respond to visual stimuli, but also to other sensory modalities, receiving subcortical facial somatosensory and auditory input from the trigeminal nuclei and the inferior colliculus respectively (e.g. Benavidez et al, 2021). The topographic map of visual space found in the sensory-related SC is impressively matched to the maps of auditory (at least for the azimuthal axis) (Ito et al, 2020) and somatosensory (Drager and Hubel, 1975) space in the motorrelated SC.…”

“…The areas involved in arrest tend to be areas connected to the optic layer in the sensory-related SC. The sensory-related SC does not extend into the most lateral quarter of SC (Benavidez et al, 2021), and the connections involved in arrest tend to be connected to the most medial three columns of SC.…”

“…V1 innervates the sensory-related SC, including the optic layer, and activation of these terminals in SC (Liang et al, 2015) or of SC neurons postsynaptic to them (Zingg et al, 2017) induces arrest, while inhibition of V1 impairs arrest to light flashes (Liang et al, 2015). By contrast, while inhibition of primary auditory cortex also impairs sound-induced arrest (Li et al, 2021), the A1 projection to SC does not innervate the optic layer (Benavidez et al, 2021), and inhibition of SC does not impair these sound-induced arrest behaviours.…”

“…Ventral to the optic layer are the 'intermediate' and then 'deep' layers, which can be collectively termed the 'motor-related SC'. Recent work suggests that the medial-lateral axis of SC can also be parcellated, into four columns that extend across layers (Benavidez et al, 2021). These columns are defined by the patterns of inputs and outputs and as yet have no known histochemical correlates.…”

“…In the case of escape, DRD2+ and PITX2+ neurons both have patchy labelling in the intermediate layer of SC, but have different projections, and activation of the former can trigger escape, suggesting that some intermediate layer neurons are involved in triggering escape (Masullo et al, 2019;Montardy et al, 2021;Xie et al, 2021). However, deep layers of SC alone are innervated by VMHdm/c (Benavidez et al, 2021), and dPAG also gets more input from the deep layers of SC than intermediate layers (Evans et al, 2018). VMHdm/c and dPAG have roles in triggering behaviour, so their connection to the deep rather than intermediate SC would suggest the deep layers are more important in triggering these behaviours.…”