Environmental factors contribute to several protein aggregation diseases, however the cause-to-effect relationships remain challenging to study. Here, we genetically abrogate sensory perception in Caenorhabditis elegans to understand the role of neuronal function in governing protein homeostasis. We reveal that defects in neuronal cilia formation reduce signaling via the thermosensory AFD neuron and alleviates protein aggregation. In contrast, ciliary mutants create an aberrant signal emanating from AFD, via the neuropeptide FLP-3 and the insulin-like peptide INS-5, blocking ubiquitin-dependent protein turnover in intestinal cells. Interestingly, lack of the calcineurin A ortholog shifts the balance from insulin towards calcineurin signaling. While both pathways are dispensable during normal sensation, the presence of a neuronal signal triggered by defective cilia primes non-neuronal cells to remodel their protein degradation pathways. In conclusion, our model elucidates the impact of environmental sensation to coordinate the balance between insulin and calcineurin signaling to maintain cellular proteostasis.