Visual information can have different meanings across species and the same visual stimulus can drive appetite or avoidance behavior. The superior colliculus, a visual center located in the midbrain has been involved in driving such behaviors. Within this structure, the wide-field-vertical cells (WFV), a conserved morphological cell-types, has been found in reptiles to highly visual mammals. Here we report our investigation of the connectivity of the WFV, their visual response properties and how these responses are modulated by locomotion in the laboratory mouse. We also address the molecular definition of these cells and attempt to reconcile recent molecular definitions acquired by single-cell and single-nucleus RNA sequencing of the SC with the NTSR1-Cre GN209 transgenic mouse line which was previously used to investigate WFV neurons. We use viral strategies to reveal WFV inputs and outputs and confirmed their unique response properties using in vivo two-photon imaging. Among the stimuli tested, WFV preferred looming and a small moving spot and displayed a bias for upward direction. When assessing the effect of locomotion, we found that only visual responses driven by a looming stimulus showed a significant change. We identified several inputs to the WFV as potential candidate for this modulation. These results suggest that WFV integrate information across multiple brain regions and are subject to behavioral modulation. Taken together, our results pave the way to elucidate the role of these neurons in visual behavior and allow us to interrogate the definition of cell-types in the light of new molecular definitions.