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

Abstract

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.

Social behavior and aging: A fly model

“…228 In contrast, another study using courtship conditioning found learning and shortterm memory deficits at 20 days of aging in a D. melanogaster model of Fragile-X syndrome compared to control flies. 230,231 The primary aim of these two studies was to show age-related deficits in an amyloid-β overexpressing Alzheimer's disease model or in hormonal signaling impaired flies, respectively. 230,231 The primary aim of these two studies was to show age-related deficits in an amyloid-β overexpressing Alzheimer's disease model or in hormonal signaling impaired flies, respectively.…”

“…229 Likewise, two recent papers reported contradictory results to the aforementioned studies in that they observed reduced short-term courtship memory even in control flies as early as 11 days of age. 230,231 The primary aim of these two studies was to show age-related deficits in an amyloid-β overexpressing Alzheimer's disease model or in hormonal signaling impaired flies, respectively. 230,231 As such, neither of these studies used non-transgenic flies (eg, Canton-S 70 ) as their control.…”

“…230,231 The primary aim of these two studies was to show age-related deficits in an amyloid-β overexpressing Alzheimer's disease model or in hormonal signaling impaired flies, respectively. 230,231 As such, neither of these studies used non-transgenic flies (eg, Canton-S 70 ) as their control. Whether the presence of transgenic alterations or methodological differences underlies the dissimilar findings among groups that have studied short-term courtship memory is currently unknown.…”

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

“…The list contained an orthologue to the gene encoding ETHR. This gene encodes two isoforms of a G protein‐coupled receptor (Park, Kim, Dupriez, & Adams, ) that mediate JH signalling in adult flies (Lee et al, ; Meiselman et al, ). Chronologically, this gene was up‐regulated at ages 3 and 6 days, then down‐regulated in the oldest group (age 12 days), but still expressed at a higher level than the age 0 day group (Figure a).…”

Omics approaches to study juvenile hormone synthesis

“…Corpora allata specific promoters have been identified and used to modify JH synthesis, or to study different aspects of CA physiology in D. melanogaster [70]. In recent studies, two different genotypes Aug21-Gal4 > UAS-GCaMP3 and JHAMT-Gal4 > UASGCaMP5 were used to detect calcium mobilization inside the CA as a result of ETH treatment [56,57]. …”