Metabolic decline in an insect ear: correlative or causative for age-related auditory decline?

• Published in: Frontiers in cell and developmental biology Vol. 11; p. 1138392
• Main Authors: Austin, Thomas T, Thomas, Christian L, Lewis, Clifton, Blockley, Alix, Warren, Ben
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Media S.A 18-05-2023
• Subjects: aging; audition (physiology); Cell and Developmental Biology; insect hearing; metabolism; sensory decline; sensory decline; metabolism; aging; insect hearing; audition (physiology)
• ISSN: 2296-634X; 2296-634X
• DOI: 10.3389/fcell.2023.1138392

One leading hypothesis for why we lose our hearing as we age is a decrease in ear metabolism. However, direct measurements of metabolism across a lifespan in any auditory system are lacking. Even if metabolism does decrease with age, a question remains: is a metabolic decrease a cause of age-related auditory decline or simply correlative? We use an insect, the desert locust
, as a physiologically versatile model to understand how cellular metabolism correlates with age and impacts on age-related auditory decline. We found that auditory organ metabolism decreases with age as measured fluorometrically. Next, we measured the individual auditory organ's metabolic rate and its sound-evoked nerve activity and found no correlation. We found no age-related change in auditory nerve activity, using hook electrode recordings, and in the electrophysiological properties of auditory neurons, using patch-clamp electrophysiology, but transduction channel activity decreased. To further test for a causative role of the metabolic rate in auditory decline, we manipulated metabolism of the auditory organ through diet and cold-rearing but found no difference in sound-evoked nerve activity. We found that although metabolism correlates with age-related auditory decline, it is not causative. Finally, we performed RNA-Seq on the auditory organs of young and old locusts, and whilst we found enrichment for Gene Ontology terms associated with metabolism, we also found enrichment for a number of additional aging GO terms. We hypothesize that age-related hearing loss is dominated by accumulative damage in multiple cell types and multiple processes which outweighs its metabolic decline.