Introduction: The evolutionarily conserved Superior Colliculus (SC) is a midbrain region essential for multisensory integration and motor responses¹. It is a highly-organised layered structure receiving inputs from different sensory modalities and connected to multiple brain regions including cortex, midbrain and brainstem². Its dysfunction has been implicated in neurodevelopmental disorders like autism and attention deficit hyperactivity disorders^3,4. Research continues to discover unique functions and novel cell populations in the mouse SC, for example its role in a secondary visual pathway bypassing the visual cortex⁵. However, how cell-type diversity is generated throughout development is still unknown despite the characterisation of radial glia progenitors (RGPs) in 1992 in the analogous structure in the chick⁶. Aim: The aim of this study is to determine the precise lineage programme instructing radial glia progenitors (RGPs) to generate SC cell-type diversity. Methods: We combined in-silico transcriptomic analyses, Mosaic Analysis with Double Markers (MADM)-based clonal analysis with single-cell RNA-sequencing to define SC development at single RGP level. Statistical analyses were performed using ANOVA, t-test, and Chi-squared test. All experiments received ethical approval from Austrian authorities. Results: We have uncovered a precise map of RGP behaviour, division patterns and potential in generating neurons, astrocytes and oligodendrocytes throughout development at single-progenitor resolution. Our data showed that individual SC RGPs are exceptionally multipotent and have the capacity to generate the full spectrum of cell-type diversity including all excitatory and inhibitory neuronal cell-types, astrocytes and oligodendrocytes in the SC. We also found that cell-type diversity is regulated by Pten, a key autism risk gene⁷. Conclusions: The delineation of the concerted production of neurons and glia during SC development provides important insights into how sensory processing is established during development and how it can be disrupted leading to lasting neurological defects.