Aging of the sensory nervous system in C. elegans

Microtubule-based sensory cilia are unique signaling compartments in the sensory neurons that transform environmental cues into sensory perception. Deterioration in sensory function is a common manifestation of aging. To provide a detailed description of ciliary morphology during neuronal aging, we focus on C. elegans amphid sensory neurons. Consistent with our previous findings in aging mechanosensory neurons, we find widespread morphological changes in multiple classes of sensory cilia in the amphid, including reduced microvilli and engorged cilia in the AFD thermosensory neuron, distorted cilia in the AWB and AWC olfactory neurons, and enlarged periciliary membrane compartments in the ASE and ASI chemosensory neurons. Aging of the AFD endings is associated with deterioration in thermosensory behaviors. Insterestingly, we observe age-related defects in the amphid sheath cells, glial cells that ensheath the AFD, AWB and AWC neurons. Overexpression of the TAX-4 cation channel or elimination of the GCY-8 receptor type guanylyl cyclase ameliorate age-dependent defects of the AFD sensory endings, suggesting that neuronal activity and glial influence contribute to the maintenance of sensory endings during aging. Taken together, our observations indicate that C. elegans sensory cilia undergo age-dependent deterioration in morphology and functions, which may represent one of the earliest aging signs of the sensory neurons.