The tectum/superior colliculus as the vertebrate solution for spatial sensory integration and action

Abstract

The superior colliculus, or tectum in the case of non-mammalian vertebrates, is a part of the brain that registers events in the surrounding space, often through vision and hearing, but also through electrosensation, infrared detection, and other sensory modalities in diverse vertebrate lineages. This information is used to form maps of the surrounding space and the positions of different salient stimuli in relation to the individual. The sensory maps are arranged in layers with visual input in the uppermost layer, other senses in deeper positions, and a spatially aligned motor map in the deepest layer. Here, we will review the organization and intrinsic function of the tectum/superior colliculus and the information that is processed within tectal circuits. We will also discuss tectal/superior colliculus outputs that are conveyed directly to downstream motor circuits or via the thalamus to cortical areas to control various aspects of behavior. The tectum/superior colliculus is evolutionarily conserved among all vertebrates, but tailored to the sensory specialties of each lineage, and its roles have shifted with the emergence of the cerebral cortex in mammals. We will illustrate both the conserved and divergent properties of the tectum/superior colliculus through vertebrate evolution by comparing tectal processing in lampreys belonging to the oldest group of extant vertebrates, larval zebrafish, rodents, and other vertebrates including primates. ''The tectum/SC's intrinsic networks, and the computations that they perform'', to the sensory and sensorimotor integration ll

Spatial Cognition in Teleost Fish: Strategies and Mechanisms

“…Some of these systems are shared with other vertebrates and seem to correspond to an ancestral design well-conserved in the different vertebrate radiations. This appears to be the case for the vestibular system, that provides a “sense of position” encoded in egocentric frames of reference anchored to the invariant direction of the gravity field and that also provide the sensory basis for inertial navigation [ 113 , 114 , 115 , 116 ], or for the optic tectum networks, that provide common body-centered frames of reference for multisensory integration and for sensory-motor transformations [ 112 , 117 , 118 ]. On the contrary, other systems are typical of fishes, for example the lateral line sensory system [ 23 , 24 , 25 ], or constitute notable examples of adaptive specializations, e.g., the electrosensory mechanisms that likely contribute to fish orientation [ 26 , 27 , 28 , 29 , 119 ].…”

Functional Organisation of the Mouse Superior Colliculus

“…Lamprey, fish and flies turn away from threatening stimuli, and in lamprey and fish, this action is supported by ipsiversive movementpromoting neurons in homologues of SC (Isa et al, 2021). Instead, mice turn towards a refuge (when present) when they are confronted by imminent threats.…”

“…The purpose of this review is to both collate this recent work and to synthesise it. While the themes we will touch on are likely to be common across species, a comparative analysis is beyond our scope, and we direct the reader to excellent recent reviews (May, 2006;Basso, Bickford and Cang, 2021;Isa et al, 2021).…”

Mechanisms of functional plasticity in subcortical visual areas

“…In the mammalian visual system, the dorsal lateral geniculate nucleus (dLGN), a primary recipient structure of retinal inputs at the thalamic level, and the superior colliculus (SC), a lamellar structure involved in the comparison of multi-modal sensory information, constitute the main subcortical visual areas and occupy complementary functions. While the dLGN is involved in precise and conscious vision [1][2][3], the SC is responsible for initiation of eye and head movements towards specific objects [4][5][6][7]. Both structures receive direct inputs from retinal ganglion cells and from the primary visual cortex and communicate with each other (Figure 1A-B).…”

“…The SC is the mammalian equivalent to the optic tectum in inferior vertebrates [5]. While many studies report functional and synaptic plasticity in tadpole optic tectum [41][42][43][44], fewer investigations have been made on the mammalian SC.…”