Pathogenic variants in the CACNA1F gene, encoding retinal Cav1.4 L-type calcium channels can lead to a spectrum of altered functional channel activity, affecting the transmission of visual signals from photoreceptors to bipolar cells. Here, we investigated the effect of the Cav1.4 C-terminal truncation variant R1827X (RX) - lacking an intramolecular mechanism, necessary for continuous calcium influx- in mouse retinas and compared the phenotype to the apparent Cav1.4 gain-of-function variant I745T (IT). Whereas the significant decrease in the Cav1.4 protein can be attributed to a loss of photoreceptors in the IT variant, photoreceptors were preserved in the RX retinas. The changes in the presynaptic terminals had an impact on the postsynaptic neurons, as evidenced by the sprouting of neurites in rod bipolar and horizontal cells on both RX and IT. However, the morphology of RX cone bipolar cell dendrites was mostly unchanged, indicating that the main impact is on the rod pathway; an effect not seen in IT. Functional analysis (i.e. electroretinograms and multielectron array analyses) supported this observation. We hypothesised that the phenotype in RX mice might be explained by a difference in protein interactions between rod and cone photoreceptors. Having established label-free mass spectrometry-based proteomics, we found several dysregulated clusters comprising e.g. retinal degeneration or synapse interaction, but also metabolism or RNA-binding proteins, differ in the IT and RX retinas that could bear an explanation for the phenotypic differences. Further investigations will include interactome analysis to better understand the molecular role of the Cav1.4 C-terminus in retinal synapse organisation.