Huntington’s Disease (HD) is a neurodegenerative disorder characterised by severe motor disturbances resulting from neural network alterations, particularly evident in deficits in oculomotor functions during the prodromic stage. The superior colliculus (SC) plays a crucial role in integrating visual perception and oculomotor functions, and recent observations in the R6/1 HD mouse model from our group indicate affected connectivity between the M2 motor cortex (M2) and SC. To comprehensively assess changes in HD pathophysiology, we conducted fMRI-based functional connectivity analysis in 17-week-old (w) wild-type (WT) and symptomatic HD mouse models. Results illuminated robust SC connectivity with various regions, such as the periaqueductal grey, cingulate, and retrosplenial cortices, showcasing notable alterations in HD mice. The onset of sensory-induced symptoms was explored using the robo-beetle test at distinct stages (8-w presymptomatic, 12-w with early motor learning deficits, and 16-w with late motor coordination deficits), coupled with ongoing biochemical assessments tracking neuronal population expression and layer distribution changes in the SC. Importantly, analyses unveiled the earlier initiation of sensory-induced symptoms in HD females at 8-w, while both sexes displayed increased tolerance and decreased avoidance and approach responses from 12-w onwards. Additionally, employing fibre photometry, we assessed neuronal activity through fluorescent calcium recordings in the M2 and SC, exposing that visual stimuli activate M2 cortex neurons in WT but not HD mice. Our data unravels the gradual temporal progression of SC-related sensorimotor deficits and cellular changes at different disease stages. This understanding is crucial for developing disease-modifying strategies targeting the early phases of HD.