4.5 Article

Distinct Aging-Vulnerable and -Resilient Trajectories of Specific Motor Circuit Functions in Oxidation- and Temperature-Stressed Drosophila

Journal

ENEURO
Volume 9, Issue 1, Pages -

Publisher

SOC NEUROSCIENCE
DOI: 10.1523/ENEURO.0443-21.2021

Keywords

escape circuit; flight; habituation; oxidative stress; seizure; temperature stress

Categories

Funding

  1. University of Iowa Biological Sciences Funding Program Grant
  2. National Institutes of Health (NIH) [GM-088804, AG-047612, AG-051513]
  3. NIH Predoctoral National Research Service Award [NS-082001]
  4. Iowa Neuroscience Institute Post-Doctoral Fellowships

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In this study, different motor circuits in Drosophila were examined, revealing distinct neurophysiological changes during aging. The research focused on the giant fiber circuit and the afferent circuits driving flight motoneuron activities, and identified different aging trajectories in their functional properties. Additionally, it was found that the aging trajectories in flies reared at high temperature were similar to those in flies reared at normal temperature over a compressed time scale. Furthermore, lifespan reduction in mutant flies was accompanied by alterations in motor circuit properties different from those in flies reared at high temperature.
In Drosophila, molecular pathways affecting longevity have been extensively studied. However, corresponding neurophysiological changes underlying aging-related functional and behavioral deteriorations remain to be fully explored. We examined different motor circuits in Drosophila across the life span and uncovered distinctive age-resilient and age-vulnerable trajectories in their established functional properties. In the giant fiber (GF) and downstream circuit elements responsible for the jump-and-flight escape reflex, we observed relatively mild deterioration toward the end of the life span. In contrast, more substantial age-dependent modifications were seen in the plasticity of GF afferent processing, specifically in use dependence and habituation properties. In addition, there were profound changes in different afferent circuits that drive flight motoneuron activities, including flight pattern generation and seizure spike discharges evoked by electroconvulsive stimulation. Importantly, in high-temperature (HT)-reared flies (29 degrees C), the general trends in these age-dependent trajectories were largely maintained, albeit over a compressed time scale, lending support for the common practice of HT rearing for expediting Drosophila aging studies. We discovered that shortened life spans in Cu/Zn superoxide dismutase (Sod) mutant flies were accompanied by altered aging trajectories in motor circuit properties distinct from those in HT-reared flies, highlighting differential effects of oxidative versus temperature stressors. This work helps to identify several age-vulnerable neurophysiological parameters that may serve as quantitative indicators for assessing genetic and environmental influences on aging progression in Drosophila.

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