Hormonal Signaling Cascade during an Early-Adult Critical Period Required for Courtship Memory Retention in Drosophila

Formation and expression of memories are critical for context-dependent decision making. In Drosophila, a courting male rejected by a mated female subsequently courts less avidly when paired with a virgin female, a behavioral modification attributed to “courtship memory.” Here we show the critical r...

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Published in:Current biology 2017-09, Vol.27 (18), p.2798-2809.e3
Main Authors: Lee, Sang Soo, Ding, Yike, Karapetians, Natalie, Rivera-Perez, Crisalejandra, Noriega, Fernando Gabriel, Adams, Michael E.
Format: Article
Language:English
Subjects:
Animals
Courtship
courtship conditioning
dopamine
Drosophila melanogaster - physiology
ecdysis triggering hormone
Insect Hormones - metabolism
juvenile hormone
Juvenile Hormones - metabolism
learning
Male
Memory
Sexual Behavior, Animal
Signal Transduction
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Summary:Formation and expression of memories are critical for context-dependent decision making. In Drosophila, a courting male rejected by a mated female subsequently courts less avidly when paired with a virgin female, a behavioral modification attributed to “courtship memory.” Here we show the critical role of hormonal state for maintenance of courtship memory. Ecdysis-triggering hormone (ETH) is essential for courtship memory through regulation of juvenile hormone (JH) levels in adult males. Reduction of JH levels via silencing of ETH signaling genes impairs short-term courtship memory, a phenotype rescuable by the JH analog methoprene. JH-deficit-induced memory impairment involves rapid decay rather than failure of memory acquisition. A critical period governs memory performance during the first 3 days of adulthood. Using sex-peptide-expressing “pseudo-mated” trainers, we find that robust courtship memory elicited in the absence of aversive chemical mating cues also is dependent on ETH-JH signaling. Finally, we find that JH acts through dopaminergic neurons and conclude that an ETH-JH-dopamine signaling cascade is required during a critical period for promotion of social-context-dependent memory. [Display omitted] •ETH-JH cascade in adult males regulates short-term courtship memory retention•JH is required for retention of memory from pheromone-independent experiences•The action of JH on memory has an early-adult-specific critical period•JH targets DA neurons to regulate male courtship memory Neuroendocrine interactions are important regulators of animal behavior. Lee et al. show that an ETH-JH-dopamine signaling cascade is required for male Drosophila memory retention by utilizing a short-term courtship-conditioning paradigm. The influence of juvenile hormone on dopamine neurons is confined to early adulthood.
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2017.08.017