Cortical projections to the superior colliculus in grey squirrels (Sciurus carolinensis)

Abstract

The superior colliculus is an important midbrain structure involved with integrating information from varying sensory modalities and sending motor signals to produce orienting movements towards environmental stimuli. Because of this role, the superior colliculus receives a multitude of sensory inputs from a wide variety of subcortical and cortical structures. Proportionately, the superior colliculus of grey squirrels is among the largest in size of all studied mammals, suggesting the importance of this structure in the behavioural characteristics of grey squirrels. Yet, our understanding of the connections of the superior colliculus in grey squirrels is lacking, especially with respect to possible cortical influences. In this study, we placed anatomical tracer injections within the medial aspect of the superior colliculus of five grey squirrels (Sciurus carolinensis) and analysed the areal distribution of corticotectal projecting cells in flattened cortex. V1 projections to the superior colliculus were studied in two additional animals. Our results indicate that the superior colliculus receives cortical projections from visual, higher order somatosensory, and higher order auditory regions, as well as limbic, retrosplenial and anterior cingulate cortex. Few, if any, corticotectal projections originate from primary motor, primary somatosensory or parietal cortical regions. This distribution of inputs is similar to the distribution of inputs described in other rodents such as rats and mice, yet the lack of inputs from primary somatosensory and motor cortex is features of corticotectal inputs more similar to those observed in tree shrews and primates, possibly reflecting a behavioural shift from somatosensory (vibrissae) to visual navigation.

Unraveling circuits of visual perception and cognition through the superior colliculus

“…That many mammals have fewer distinguishable superficial layers than some reptiles and birds may stem from the nocturnal origins of mammals, when carnivorous reptiles inhabited the earth, as well as the increased reliance on vision for flight in birds (Knudsen, 2020;Northcutt, 2002;Stein and Gaither, 1981). Many of the comparisons made between the layers of the tectum of different vertebrate species used diurnal, highly visual reptiles and birds and crepuscular or nocturnal mammals, such as the cat and some species of rodent, such as the hamster (Baldwin and Kaas, 2012;Baldwin et al, 2013bBaldwin et al, , 2019Chalupa and Rhoades, 1977;Harting and Guillery, 1976;Harting et al, 1992;Rhoades et al, 1987;Vanegas, 1984). More detailed comparisons across species with similar visual capabilities (e.g., binocularity and stereopsis or color vision) combined with modern molecular methods for identifying neuronal cell types is a rich area for future investigation to explore the evolution of the SC, its layers, and its neuronal cell types.…”

Neuroplasticity and crossmodal connectivity in the normal, healthy brain.

“…The SC deep layers and other subcortical structures (e.g., the caudate nucleus, and substantia nigra in the basal ganglia; Nagy et al, 2006) are strongly connected to the thalamus and several other brain areas (May, 2006). These layers receive stimuli from somatosensory, auditory, and visual cortices (e.g., Alvarado et al, 2009; Baldwin et al, 2019; Meredith & Stein, 1983, 1986; Rowland, Quessy, et al, 2007; Stein & Arigbede, 1972; Wallace, 2004; Wallace et al, 1993, 1996, Wallace & Stein, 1996, 2001). However, it is still unknown whether they send any feedback projections to these sensory cortices (Figure 2b, j).…”

Dopamine modulates visual threat processing in the superior colliculus via D2 receptors

“…Finally, to determine the source of dopaminergic modulation in the SC, we injected the retrograde tracer cholera toxin B (CTB) into the SC (Figure S3A). CTB tracer was found in structures such as the primary visual cortex and the anterior cingulate cortex, both known to project to the SC (Baldwin et al, 2019;Zingg et al, 2017) (Figures S3B1 and SB2). CTB tracer was also found in the ventral tegmental area (VTA), the substantia nigra (SN), the periaqueductal gray (PAG), the paraventricular nucleus of the hypothalamus (PVN), or the dorsal raphe nucleus (DRN), known to synthetize DA (Bjo ¨rklund and Dunnett, 2007) (Figures S3C1-S3C5, S3D1).…”