The Superior Colliculus: Cell Types, Connectivity, and Behavior

Abstract

The superior colliculus (SC), one of the most well-characterized midbrain sensorimotor structures where visual, auditory, and somatosensory information are integrated to initiate motor commands, is highly conserved across vertebrate evolution. Moreover, cell-type-specific SC neurons integrate afferent signals within local networks to generate defined output related to innate and cognitive behaviors. This review focuses on the recent progress in understanding of phenotypic diversity amongst SC neurons and their intrinsic circuits and long-projection targets. We further describe relevant neural circuits and specific cell types in relation to behavioral outputs and cognitive functions. The systematic delineation of SC organization, cell types, and neural connections is further put into context across species as these depend upon laminar architecture. Moreover, we focus on SC neural circuitry involving saccadic eye movement, and cognitive and innate behaviors. Overall, the review provides insight into SC functioning and represents a basis for further understanding of the pathology associated with SC dysfunction.

Layer-dependent activity in the human superior colliculus during working memory

“…The layer-dependent pattern of the SC BOLD intensity we observed in SC BOLD intensity was replicated using a data-driven approach that showed distinct connectivity patterns of the superficial and deep layers of the SC, such that the superficial layers of SC showed strong functional connectivity with cortical and subcortical structures important for visual processing, while deep layers of SC showed strong functional connectivity with cortical and subcortical structures important for a more diverse set of functions, including visceromotor control and executive function. These results are consistent with the well-established anatomical and functional evidence in non-human vertebrates that the superficial layers are exclusively visual, and in contrast, multimodal sensory, motor, and cognitive functions are localized in the intermediate and deep layers (Liu et al, 2022).…”

“…The superior colliculus (SC) is a laminated structure in the vertebrate midbrain with three distinct anatomical layers along a dorsolateral to ventromedial axis (May, 2006). Anatomical and behavioral evidence from non-human vertebrates indicates that the superficial layers are primarily visual sensory in nature, whereas the intermediate and deep layers are multisensory and contribute to both skeletomotor and visceromotor control (for review, see Gandhi & Katnani, 2011; Liu et al, 2022), coordinating fast motor outputs in threatening and appetitive encounters (see Isa et al, 2021). Research in non-human vertebrates further supports a role for the intermediate and deep layers of SC in selective attention (e.g., Lovejoy & Krauzlis, 2010) and perceptual decision-making (e.g., Jun et al, 2021; for review, see Basso et al, 2021).…”

Monosynaptic trans-collicular pathways link mouse whisker circuits to integrate somatosensory and motor cortical signals

“…The SC contains substantial populations of GABAergic neurons with reported numbers ranging from 30% to 45% [15]. We estimate that the LSC contains ∼23% GABAergic neurons.…”

“…However, these mesoscopic modules comprise intermingled populations of input and output neurons as well as input neurons with different input identities [15–17], for example, retinal and cortical inputs [18]. Therefore, dissection of input-defined cell-types and analysis of their outputs is critical to unambiguously link specific SC input pathways to specific SC downstream targets and to determine whether cortical input signals can be transformed directly into SC output to downstream SC target circuits. The SC comprises excitatory and inhibitory neurons; for example, in the visual SC approximately one third of the neurons are GABAergic [14,19]. However, very little is known about GABAergic neurons in the somatosensory SC (Fig.…”

“…While intra-collicular circuits are well-described [13], evidence for monosynaptic trans-collicular pathways is limited because relatively few studies have delineated the precise input-output connectivity of defined subpopulations in SC [2,14]. Indeed, input-output connectivity of the SC is mostly considered at the level of SC layers [2,15] and radial cortico-collicular input zones [16]. However, these mesoscopic modules comprise intermingled populations of input and output neurons as well as input neurons with different input identities [16][17][18], for example, retinal and cortical inputs [19].…”