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

Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843-3258, USA.
Neurobiology of aging (Impact Factor: 5.01). 01/2012; 33(7):1483.e5-23. DOI: 10.1016/j.neurobiolaging.2011.12.016
Source: PubMed


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, Ca(2+) 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 acetylcholine receptor (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.

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    • "Until recently, it was thought that C. elegans neurons did not show age-related morphological decline at either a cellular or subcellular level, because while other tissues, such as skin and muscle, deteriorate with age (Garigan et al., 2002), neurons remained surprisingly intact (Herndon et al., 2002). These data seem counterintuitive, considering multiple sensory behaviors as well as motility decline with age in C. elegans (Glenn et al., 2004; Murakami et al., 2005; Hsu et al., 2009; Kauffman et al., 2010; Guo et al., 2012) and changes in dendritic spines and synapse number with age have been observed in other organisms, including non-human primates and rats (reviewed in Burke and Barnes, 2006; Morrison and Baxter , 2012). Due to this incongruity, recent work has again tested the integrity of neurons and found that while neuronal cell bodies stay intact, neuronal processes, subcellular structures (Pan et al., 2011; Tank et al., 2011; Toth et al., 2012), and neuronal activity (Chokshi et al., 2010; Mulcahy et al., 2012) all show age-dependent changes. "
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    Frontiers in Genetics 11/2012; 3:259. DOI:10.3389/fgene.2012.00259
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    ABSTRACT: Author Summary An animal's behavior is a complex output displayed in response to diverse external cues, which are sensed and processed by the nervous system. Nerve cells translate sensory information into chemical secretions (neurotransmitters). These chemical signals allow neurons and muscles to communicate and coordinate motor responses. However, it is complicated how these signals are interpreted in neuronal circuits to start, continue, modify, and end specific behaviors, under the appropriate conditions. The neurotransmitter dopamine (DA) is involved in adjusting animal movements, thus DA neurotransmission is a candidate for coupling behaviors to the proper situational context. Here, we used C. elegans copulation to understand the DA-regulated neuronal mechanisms that promote when and where motor responses should be executed. During mating, DA is used as a feedback mechanism to adjust the activity of multiple sensory-motor neurons and muscles that promote the rhythmic thrusting of the male copulatory organs against his partner's vulval genitalia. If vulval signals are withdrawn when the male loses contact with his mate's genitalia, the DA-adjusted motor neurons' activities dampen to cease cue-independent genital penetration attempts. Therefore, DA secretions fine-tune these motor outputs to be exclusively displayed at the vulva and thus confine a behavior to its corresponding context.
    PLoS Genetics 11/2012; 8(11):e1003015. DOI:10.1371/journal.pgen.1003015 · 7.53 Impact Factor
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    ABSTRACT: Although much is known about female reproductive aging, fairly little is known about the causes of male reproductive senescence. We developed a method that facilitates culture maintenance of C. elegans adult males, which enabled us to measure male fertility as populations age, without profound loss of males from the growth plate. We find that the ability of males to sire progeny declines rapidly in the first half of adult lifespan and we examined potential factors that contribute towards reproductive success, including physical vigor, sperm quality, mating apparatus morphology, and mating ability. Of these, we find little evidence of general physical decline in males or changes in sperm number, morphology, or capacity for activation, at time points when reproductive senescence is markedly evident. Rather, it is the loss of efficient mating ability that correlates most strongly with reproductive senescence. Low insulin signaling can extend male ability to sire progeny later in life, although insulin impact on individual facets of mating behavior is complex. Overall, we suggest that combined modest deficits, predominantly affecting the complex mating behavior rather than sperm quality, sum up to block effective C. elegans male reproduction in middle adult life.
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