The mushroom body D1 dopamine receptor controls innate courtship drive

Abstract

Mating is critical for species survival and is profoundly regulated by neuromodulators and neurohormones to accommodate internal states and external factors. To identify the underlying neuromodulatory mechanisms, we investigated the roles of dopamine receptors in various aspects of courtship behavior in Drosophila. Here we report that the D1 dopamine receptor dDA1 regulates courtship drive in naïve males. The wild-type naïve males actively courted females regardless their appearance or mating status. On the contrary, the dDA1 mutant (dumb) males exhibited substantially reduced courtship toward less appealing females including decapitated, leg-less and mated females. The dumb male’s reduced courtship activity was due to delay in courtship initiation and prolonged intervals between courtship bouts. The dampened courtship drive of dumb males was rescued by reinstated dDA1 expression in the mushroom body α/β and γ neurons but not α/β or γ neurons alone, which is distinct from the previously characterized dDA1 functions in experience-dependent courtship or other learning and memory processes. We also found that the dopamine receptors dDA1, DAMB and dD2R are dispensable for associative memory formation and short-term memory of conditioned courtship, thus courtship motivation and associative courtship learning and memory are regulated by distinct neuromodulatory mechanisms. Taken together, our study narrows the gap in the knowledge of the mechanism that dopamine regulates male courtship behavior.

Social behavior and aging: A fly model

“…Overall, most genes' expression in the brain decreases with age in D. melanogaster, as shown by a recent extensive single-cell sequencing of the transcriptome in brains of young vs old males and females (1 vs 50 days of age). 86 Age-related declines in whole body levels of DA and corresponding changes in dopaminergic-modulated behaviors during rituals have been reported. 77 However, the functional significance on longevity of each of these genes remains to be elucidated.…”

“…79,80 These neurons play an important role in the regulation of insects' energy metabolism, adaptation to environmental stresses, 81,82 orientation control, 83 differentiating between aversive and appetitive olfactory memories in D. melanogaster, 84 and motivation/reward pathways, 85 including courtship drive. 86 Age-related declines in whole body levels of DA and corresponding changes in dopaminergic-modulated behaviors during rituals have been reported. 87,88 Some studies report decrease in dopaminergic cells viability with age, 78 while other do not.…”

Drosophila mef2is essential for normal mushroom body and wing development

“…The axonal lobes are segregated into domains according to their interconnections with distinct types of dopaminergic neurons and cholinergic mushroom body output neurons (Aso et al, 2014). Numerous genes required for normal olfactory learning are preferentially expressed in the MBs, often in subsets of axonal lobes that likely reflects their distinct functions (McGuire et al, 2001;Yu et al, 2006;Krashes et al, 2007;Akalal et al, 2010;DasGupta et al, 2014;Lim et al, 2017). The role of D-mef2 in MB development and function remains untested.…”

Nuclear transcriptomes of the seven neuronal cell types that constitute theDrosophilamushroom bodies

“…An arsenal of genetic tools to manipulate any gene's function within each of these cell subtypes already exists (109,110). In addition to olfactory associative memory, MBs also play fundamental roles in other forms of memory including visual and gustatory (9, 10), temperature preference (11), courtship behaviors (79,80), stress response (92), food-seeking (111), sleep (12) and responses to ethanol (13). This dataset will facilitate the discovery of neural mechanisms for each of these conserved behaviors.…”

“…, regulated forgetting(76,77), sleep(78), courtship behaviors(79,80), and temperature preference(81). A network of dopaminergic neurons innervates all MB cell subtypes(17), and all four dopamine receptors, Dop1R1, Dop1R2, Dop2R and DopEcR, are expressed in all 7 MB KC subtypes (594 -1152, 222 -408, 444 -1059, 3284 -8335 TPM, respectively;Figure 5B)(28, 71, 82, 83; cf 84).…”