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The Journal of Neuroscience, November 23, 2005, 25(47):10894-10904; doi:10.1523/JNEUROSCI.3600-04.2005

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Neurobiology of Disease
Aging-Dependent and -Independent Modulation of Associative Learning Behavior by Insulin/Insulin-Like Growth Factor-1 Signal in Caenorhabditis elegans

Hana Murakami,^1,2 Karalee Bessinger,¹ Jason Hellmann,¹ and Shin Murakami^1,2

¹Gheens Center on Aging, Department of Biochemistry and Molecular Biology, University of Louisville School of Medicine, Louisville, Kentucky 40202, and ²Department of Dermatology and Pathology, Geriatrics Center and Institute of Gerontology, University of Michigan Medical School, Ann Arbor, Michigan 48109

Mutations in the insulin/IGF-1 neuroendocrine pathway extend lifespan and affect development, metabolism, and other biological processes in Caenorhabditis elegans and in other species. In addition, they may play a role in learning and memory. Investigation of the insulin/IGF-1 pathway may provide clues for the prevention of age-related declines in cognitive functions. Here, we examined the effects of the life-extending (Age) mutations, such as the age-1 (phosphatidylinositol 3-OH kinase) and daf-2 (insulin/IGF-1 receptor) mutations, on associative learning behavior called isothermal tracking. This thermotaxis learning behavior associates paired stimuli, temperature, and food. The age-1 mutation delayed the age-related decline of isothermal tracking, resulting in a 210% extension of the period that ensures it. The effect is dramatic compared with the extension of other physiological health spans. In addition, young adults of various Age mutants (age-1, daf-2, clk-1, and eat-2) showed increased consistency of temperature-food association, which may be caused by a common feature of the mutants, such as the secondary effects of life extension (i.e., enhanced maintenance of neural mechanisms). The age-1 and daf-2 mutants but not the other Age mutants showed an increase in temperature-starvation association through a different mechanism. Increased temperature-food association of the daf-2 mutant was dependent on neuronal Ca²⁺-sensor ncs-1, which modulates isothermal tracking in the AIY interneuron. Interestingly, mutations in the daf-7 TGF gene, which functions in parallel to the insulin/IGF-1 pathway, caused deficits in acquisition of temperature-food and temperature-starvation association. This study highlights roles of the Age mutations in modulation of certain behavioral plasticity.

Key words: aging; life extension; insulin/IGF-1 signal; stress resistance; learning and memory; behavioral plasticity

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Received Sep 1, 2004; revised October 5, 2005; accepted October 5, 2005.

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