Behavioral decay in aging male C. elegans correlates with increased cell excitability

Abstract

Deteriorative changes in behavioral functions are natural processes that accompany aging. In advanced aged C. elegans nematodes, gross decline in general behaviors, such as locomotion and feeding, is correlated with degeneration of muscle structure and contractile function. In this study, we characterized the age-related changes in C. elegans male mating behavior to determine possible causes that ultimately lead to age-related muscle frailty. Unlike the kinetics of general behavioral decline, we found that mating behavior deteriorates early in adulthood, with no obvious muscle fiber disorganization or sperm dysfunction. Through direct mating behavior observations, Ca2+ imaging and pharmacological tests, we found that the muscular components used for mating become more excitable as the males age. Interestingly, manipulating either the expression of AChR genes or dietary-mediated ether-a-go-go family K+ channel function can reduce the muscle excitability of older males and concurrently improve mating behavior, suggesting a correlation between these biological processes.

Pharmacological assays reveal age-related changes in synaptic transmission at the Caenorhabditis elegans neuromuscular junction that are modified by reduced insulin signalling

“…This analysis at distinct stages of worm ageing suggests a biphasic modulation of neuromuscular function as the worm ages from a young adult to mature adult, to an organism beyond the median point of its life expectancy. The observation of a stronger neuromuscular system during early ageing is supported by a recent study on male C. elegans, suggesting an increased excitability of the muscle cells used during mating in early ageing (Guo et al, 2012). This was coupled with the observation that the spicule muscles of males on the third day of adulthood are hypersensitive to levamisole (Guo et al, 2012).…”

“…In the latter, motility and pharyngeal nerve-muscle function appear to be in decline during a period that the pharmacological assays of neuromuscular function are suggesting improved efficacy that peaks on the fifth day of adulthood. In male worms, Guo et al (Guo et al, 2012) suggest that the hyperexcitability seen in the muscle cells used for mating during early ageing may be the basis for the decline in mating behaviour. Indeed, by genetically reducing the excitability of the muscle cells they delayed the behavioural decline (Guo et al, 2012).…”

“…In male worms, Guo et al (Guo et al, 2012) suggest that the hyperexcitability seen in the muscle cells used for mating during early ageing may be the basis for the decline in mating behaviour. Indeed, by genetically reducing the excitability of the muscle cells they delayed the behavioural decline (Guo et al, 2012). Therefore, an increased strength of neuromuscular transmission does not necessarily correlate with the ability to execute intact behaviours.…”

TMC-1 attenuates C. elegans development and sexual behaviour in a chemically defined food environment

“…The assay combines in one metric how fast males sustain, reattempt and complete insertion into the hermaphrodite vulva of their copulatory organs, the spicules 48 . When males were developed in OP50 and their various copulatory behaviours were observed on CeMM, we did not detect any difference in spicule insertion efficiency between wild type and mutant (Fig.…”

Developmental alterations of the C. elegans male anal depressor morphology and function require sex-specific cell autonomous and cell non-autonomous interactions

“…We first performed the mating potency assay by pairing a 1-day-old male with a 1-day-old hermaphrodite (Correa et al, 2012;Guo et al, 2012;Liu et al, 2011). The hermaphrodites possess the pha-1(e2123) temperature-sensitive mutation, and therefore at 20 1C only cross-progeny can survive.…”