Co-Conservation of Synaptic Gene Expression and Circuitry in Collicular Neurons

Area of Science:

• Neuroscience
• Evolutionary Biology
• Comparative Genomics

Background:

• The superior colliculus (SC) is a crucial midbrain sensorimotor hub with conserved functions across vertebrates.
• Understanding the evolution of SC cell types is essential for deciphering its conserved and divergent roles.

Purpose of the Study:

• To compare the molecular and cellular organization of the SC across species with significant evolutionary divergence.
• To identify conserved and novel neuronal subtypes and genetic elements within the SC.

Main Methods:

• Single-nucleus transcriptomics was employed to analyze the SC's cellular composition.
• Comparative analysis was performed on SC tissue from mice, tree shrews, and humans.

Main Results:

• Approximately 30 consensus neuronal subtypes were identified, including conserved Cbln2+ neurons forming the SC-pulvinar circuit.
• Synapse-related genes showed high conservation, contrasting with neocortical evolution, suggesting co-conservation of circuitry.
• Cilia-related genes exhibited significant divergence, indicating a role for the neuronal primary cilium in SC evolution.
• A novel inhibitory SC neuron subtype was discovered in tree shrews and humans, absent in mice.

Conclusions:

• The SC has evolved through the conservation of fundamental neuron subtypes and synaptic genes, alongside the diversification of ciliary gene expression.
• The identification of a novel inhibitory neuron subtype highlights species-specific adaptations within the SC.
• These findings provide insights into the evolutionary mechanisms shaping this vital midbrain structure.