Effects of Sex and Insulin/Insulin-Like Growth Factor-1 Signaling on Performance in an Associative Learning Paradigm in<i>Caenorhabditis elegans</i>

Vellai, Tibor; McCulloch, Diana; Gems, David; Kovács, Attila

doi:10.1534/genetics.106.061499

Cited by 41 publications

(34 citation statements)

References 50 publications

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“…They proposed that this sex-based learning deficit was the result of reduced insulin/IGF-1 signaling. Consistent with this hypothesis, both Vellai et al (2006) and Tomioka et al (2006) demonstrated a role for insulin-like signaling in the modulation of NaCl preference. NaCl starvation conditioning was defective in worms with mutations in genes encoding homologs of insulin (ins-1), insulin/IGF-I receptor (daf-2), PI 3-kinase (age-1), phosphoinositide-dependent kinase (pdk-1), and Akt/PKB (akt-1).…”

Section: Taste As the Conditioned Stimulussupporting

confidence: 63%

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An elegant mind: Learning and memory in Caenorhabditis elegans

Ardiel¹,

Rankin²

2010

Learn. Mem.

275

191

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This article reviews the literature on learning and memory in the soil-dwelling nematode Caenorhabditis elegans. Paradigms include nonassociative learning, associative learning, and imprinting, as worms have been shown to habituate to mechanical and chemical stimuli, as well as learn the smells, tastes, temperatures, and oxygen levels that predict aversive chemicals or the presence or absence of food. In each case, the neural circuit underlying the behavior has been at least partially described, and forward and reverse genetics are being used to elucidate the underlying cellular and molecular mechanisms. Several genes have been identified with no known role other than mediating behavior plasticity.Historically, it was believed that even if they were capable of learning, the nervous systems of invertebrates were too different to be instructive on human cognition. In the 1960s, Kandel and colleagues began studying learning in the marine mollusc Aplysia (Kandel and Tauc 1965). Using this system, they were able to relate behavioral plasticity to changes at specific synapses of identified neurons, and began a biochemical analysis of these neuronal changes, uncovering a role for cAMP, PKA, and CREB. In the 1970s, Benzer and colleagues began a genetic dissection of learning in the fruit fly Drosophila melanogaster (Quinn et al. 1974;Dudai et al. 1976). They established an associative learning assay (Quinn et al. 1974) and conducted a forward genetic screen, identifying the first learning mutant, dunce (Dudai et al. 1976). Since then, many genes have been cloned, and the biological basis of learning has proven to be highly conserved (Barco et al. 2006;Skoulakis and Grammenoudi 2006). Today there is no question as to the relevance of invertebrate research in the field of learning and memory.At about the same time that Kandel was beginning his work with Aplysia, Sydney Brenner chose Caenorhabditis elegans as the organism in which to study development and the nervous system (Brenner 1974). Today this transparent nematode is the world's best understood animal. It's small size ( 1 mm), short life cycle (,3 d), and ease of cultivation make it perfect for the laboratory, and its mode of reproduction is ideal for genetic analysis-selffertilizing hermaphrodites can be easily inbred or crossed with males. The genome has been mapped and sequenced, and there are thousands of mutants and RNAi constructs readily available for researchers. Furthermore, C. elegans has an invariant cell lineage and relatively simple morphology-959 cells make up the entire adult hermaphrodite (Sulston and Horvitz 1977;Sulston et al. 1983). Using serial section electron micrographs, White et al. (1986) were able to construct a neural wiring diagram of the hermaphrodite's 302 neurons. They found about 5000 chemical synapses, 600 gap junctions, and 2000 neuromuscular junctions, the location of which were fairly consistent between animals. With its invariant cell lineage and reproducible connectome, C. elegans was initially viewed as a genetically hardwired ...

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Section: Taste As the Conditioned Stimulussupporting

confidence: 63%

“…Interestingly, Vellai et al (2006) found that male worms were less proficient at salt starvation learning than hermaphrodites. They proposed that this sex-based learning deficit was the result of reduced insulin/IGF-1 signaling.…”

Section: Taste As the Conditioned Stimulusmentioning

confidence: 99%

An elegant mind: Learning and memory in Caenorhabditis elegans

Ardiel¹,

Rankin²

2010

Learn. Mem.

275

191

View full text Add to dashboard Cite

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“…2 A). The plasticity deficit observed in daf-2(e1370) likely is not attributable to sensory defects, as these mutants have normal benzaldehyde sensation and starvation-induced behaviors (Vellai et al, 2006).…”

Section: Resultsmentioning

confidence: 99%

Insulin Signaling Plays a Dual Role in Caenorhabditis elegans Memory Acquisition and Memory Retrieval

Lin

Tomioka²,

Pereira³

et al. 2010

Journal of Neuroscience

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Insulin signaling plays a prominent role in regulation of dauer formation and longevity in Caenorhabditis elegans. Here, we show that insulin signaling also is required in benzaldehyde-starvation associative plasticity, in which worms pre-exposed to the odor attractant benzaldehyde in the absence of food subsequently demonstrate a conditioned aversion response toward the odorant. Animals with mutations in insulin-related 1 (ins-1), abnormal dauer formation 2 (daf-2), and aging alteration 1 (age-1), which encode the homolog of human insulin, insulin/IGF-1 receptor, and PIP3 kinase, respectively, demonstrated significant deficits in benzaldehyde-starvation associative plasticity. Using a conditional allele, we show that the behavioral roles of DAF-2 signaling in associative plasticity can be dissociated, with DAF-2 signaling playing a more significant role in the memory retrieval than in memory acquisition. We propose DAF-2 signaling acts as a learning-specific starvation signal in the memory acquisition phase of benzaldehyde-starvation associative plasticity but functions to switch benzaldehyde-sensing amphid wing C neurons into an avoidance signaling mode during memory retrieval.

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“…Another series of C. elegans studies suggests that some life-extending treatments improve cognitive function, including performance and memory function, whereas others do not (20,21). In Drosophila, dietary-restricted flies show lifespan extension but no improvement in their cognitive ability (aversion learning test) compared with wild type (22).…”

mentioning

confidence: 99%

Uncoupling lifespan and healthspan in Caenorhabditis elegans longevity mutants

Bansal¹,

Zhu

Yen³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

303

351

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Aging research has been very successful at identifying signaling pathways and evolutionarily conserved genes that extend lifespan with the assumption that an increase in lifespan will also increase healthspan. However, it is largely unknown whether we are extending the healthy time of life or simply prolonging a period of frailty with increased incidence of age-associated diseases. Here we use Caenorhabditis elegans, one of the premiere systems for lifespan studies, to determine whether lifespan and healthspan are intrinsically correlated. We conducted multiple cellular and organismal assays on wild type as well as four long-lived mutants (insulin/insulin-like growth factor-1, dietary restriction, protein translation, mitochondrial signaling) in a longitudinal manner to determine the health of the animals as they age. We find that some long-lived mutants performed better than wild type when measured chronologically (number of days). However, all long-lived mutants increased the proportion of time spent in a frail state. Together, these data suggest that lifespan can no longer be the sole parameter of interest and reveal the importance of evaluating multiple healthspan parameters for future studies on antiaging interventions.

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Effects of Sex and Insulin/Insulin-Like Growth Factor-1 Signaling on Performance in an Associative Learning Paradigm inCaenorhabditis elegans

Cited by 41 publications

References 50 publications

An elegant mind: Learning and memory in Caenorhabditis elegans

An elegant mind: Learning and memory in Caenorhabditis elegans

Insulin Signaling Plays a Dual Role in Caenorhabditis elegans Memory Acquisition and Memory Retrieval

Uncoupling lifespan and healthspan in Caenorhabditis elegans longevity mutants

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