Molecular features distinguish ten neuronal types in the mouse superficial superior colliculus

Abstract

The superior colliculus (SC) is a midbrain center involved in controlling head and eye movements in response to inputs from multiple sensory modalities. Visual inputs arise from both the retina and visual cortex and converge onto the superficial layer of the SC (sSC). Neurons in sSC send information to deeper layers of SC and to thalamic nuclei that modulate visually guided behaviors. Presently, our understanding of sSC neurons is impeded by a lack of molecular markers that define specific cell types. To better understand the identity and organization of sSC neurons, we took a systematic approach to investigate gene expression within four molecular families: transcription factors, cell adhesion molecules, neuropeptides and calcium binding proteins. Our analysis revealed 12 molecules with distinct expression patterns in mouse sSC: cadherin 7, contactin 3, netrin G2, cadherin 6, protocadherin 20, retinoid-related orphan receptor β, brain-specific homeobox/POU domain protein 3b, Ets variant gene 1, substance P, somatostatin, vasoactive intestinal polypeptide and parvalbumin. Double labeling experiments, by either in situ hybridization or immunostaining, demonstrated that the 12 molecular markers collectively define 10 different sSC neuronal types. The characteristic positions of these cell types divide sSC into 4 distinct layers. The 12 markers identified here will serve as valuable tools to examine molecular mechanisms that regulate development of sSC neuron types. These markers could also be used to examine the connections between specific cell types that form retinocollicular, corticocollicular or colliculothalamic pathways.

The sifting of visual information in the superior colliculus

“…The microcircuitry of the SC is still poorly understood, at least compared to that of the retina. One can distinguish about 5 to 10 neuronal types based on morphology and gene expression (Byun et al, 2016;Gale and Murphy, 2014), but their synaptic connectivity is largely unknown. Furthermore the SC interacts through long-range connections with other brain regions, notably the visual cortex (Seabrook et al, 2017).…”

“…Or the local looming detectors may be nonlinear dendrites, and ion channels with long-lasting inactivation (Ulbricht, 2005) may play the role of depressing synapses. The increasing availability of genetic handles for cell types in the SC (Byun et al, 2016;Gale and Murphy, 2014) should help in cracking some of these microcircuits.…”

The mouse pulvinar nucleus: Organization of the tectorecipient zones

“…However, the availability of transgenic mouse lines (e.g. Byun et al, 2016; Gale and Murphy, 2014, 2016) may help to facilitate the categorization of these cells. If subclasses of WFV cells exist in the mouse, those that extend dendrites most superficially within the SC (Figure 2C) could potentially be innervated by populations of retinal axons that are restricted to the most superficial regions of the SGS (e.g.…”

Divergent projection patterns of M1 ipRGC subtypes

“…Charting of total M1 ipRGC (Control; shown in black) and Brn3b-negative M1 ipRGC (Brn3bDTA; shown in blue) innervation to multiple brain areas plotted on coronal sections from atlas of the adult mouse brain (Franklin & Paxinos, 2008). Abbreviations for each structure are defined in Figure 6 [Color figure can be viewed at wileyonlinelibrary.com] Brn3b z-dta line (Byun et al, 2016). The sparse innervation observed in the rostral dLGN of Control mice (Figure 3g) was reduced completely (2/5) or to no more than a single fiber visible in adjacent sections in Brn3bDTA mice (3/5; Figure 3h).…”