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Sexual dimorphism in the fly brain.

ABSTRACT: BACKGROUND:Sex-specific behavior may originate from differences in brain structure or function. In Drosophila, the action of the male-specific isoform of fruitless in about 2000 neurons appears to be necessary and sufficient for many aspects of male courtship behavior. Initial work found limited evidence for anatomical dimorphism in these fru+ neurons. Subsequently, three discrete anatomical differences in central brain fru+ neurons have been reported, but the global organization of sex differences in wiring is unclear. RESULTS:A global search for structural differences in the Drosophila brain identified large volumetric differences between males and females, mostly in higher brain centers. In parallel, saturating clonal analysis of fru+ neurons using mosaic analysis with a repressible cell marker identified 62 neuroblast lineages that generate fru+ neurons in the brain. Coregistering images from male and female brains identified 19 new dimorphisms in males; these are highly concentrated in male-enlarged higher brain centers. Seven dimorphic lineages also had female-specific arbors. In addition, at least 5 of 51 fru+ lineages in the nerve cord are dimorphic. We use these data to predict >700 potential sites of dimorphic neural connectivity. These are particularly enriched in third-order olfactory neurons of the lateral horn, where we provide strong evidence for dimorphic anatomical connections by labeling partner neurons in different colors in the same brain. CONCLUSION:Our analysis reveals substantial differences in wiring and gross anatomy between male and female fly brains. Reciprocal connection differences in the lateral horn offer a plausible explanation for opposing responses to sex pheromones in male and female flies.

SUBMITTER: Cachero S

PROVIDER: S-EPMC2957842 | biostudies-literature | 2010 Sep

REPOSITORIES: biostudies-literature

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Sexual dimorphism in the fly brain.

Cachero Sebastian S Ostrovsky Aaron D AD Yu Jai Y JY Dickson Barry J BJ Jefferis Gregory S X E GS

Current biology : CB 20100909 18

<h4>Background</h4>Sex-specific behavior may originate from differences in brain structure or function. In Drosophila, the action of the male-specific isoform of fruitless in about 2000 neurons appears to be necessary and sufficient for many aspects of male courtship behavior. Initial work found limited evidence for anatomical dimorphism in these fru+ neurons. Subsequently, three discrete anatomical differences in central brain fru+ neurons have been reported, but the global organization of sex ...[more]

PMID: 20832311

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Project description:Sex differences in behavior and morphology are usually assumed to be stronger in polygynous species compared to monogamous species. A few brain structures have been identified as sexually dimorphic in polygynous rodent species, but it is less clear whether these differences persist in monogamous species. California mice are among the 5% or less of mammals that are considered to be monogamous and as such provide an ideal model to examine sexual dimorphism in neuroanatomy. In the present study we compared the volume of hypothalamic- and limbic-associated regions in female and male California mice for sexual dimorphism. We also used tyrosine hydroxylase (TH) immunohistochemistry to compare the number of dopamine neurons in the ventral tegmental area (VTA) in female and male California mice. Additionally, tract tracing was used to accurately delineate the boundaries of the VTA. The total volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA), the principal nucleus of the bed nucleus of the stria terminalis (BNST), and the posterodorsal medial amygdala (MEA) was larger in males compared to females. In the SDN-POA we found that the magnitude of sex differences in the California mouse were intermediate between the large differences observed in promiscuous meadow voles and rats and the absence of significant differences in monogamous prairie voles. However, the magnitude of sex differences in MEA and the BNST were comparable to polygynous species. No sex differences were observed in the volume of the whole brain, the VTA, the nucleus accumbens or the number of TH-ir neurons in the VTA. These data show that despite a monogamous social organization, sexual dimorphisms that have been reported in polygynous rodents extend to California mice. Our data suggest that sex differences in brain structures such as the SDN-POA persist across species with different social organizations and may be an evolutionarily conserved characteristic of mammalian brains.

Project description:Background and purposeNeonatal encephalopathy caused by hypoxia-ischemia (HI) is a major cause of death and disability in newborns. Clinical and experimental studies suggest a sexual dimorphism in HI-induced brain injury and therapy responses. A major hallmark of HI pathophysiology is the infiltration of peripheral immune cells into the injured brain. However, the specific role of regulatory T cells (Tregs) in neonatal HI is still unknown.MethodsNine-day-old mice were exposed to HI by ligation of the right common carotid artery followed by 1 hour hypoxia (10% oxygen). Using immunohistochemistry, flow cytometry, and microarray analyses, Tregs were investigated in the brain, spleen, and blood 24 hours post HI. The functional role of Tregs was evaluated by acute Treg depletion in depletion of regulatory T cells transgenic mice. Brain injury, neuroinflammatory responses, and vascular injury were analyzed via immunohistochemistry and Western blot 48 hours and 7 days after HI. Functional outcome was assessed 3 days and 5 weeks after HI.ResultsFemale mice revealed an increased cerebral Treg infiltration, coinciding with elevated chemokine receptor expression. Treg depletion in females aggravated HI-induced brain tissue injury, short-term motor deficits, and long-term deficits in exploratory activity, paralleled by an increased microglia and endothelial activation and leukocyte infiltration. Treg depletion in male mice reduced HI-induced brain injury, short-term motor, and long-term cognitive deficits, associated with reduced vascular injury. Ex vivo isolated female Tregs displayed an increased immunosuppressive activity on effector T cell proliferation and an increased gene enrichment in pathways related to enhanced Treg activity.ConclusionsTregs from neonatal female mice provide endogenous neuroprotection, whereas Tregs from male mice increase secondary neurodegeneration. As potential mechanisms, we identified intrinsic transcriptional differences associated with enhanced anti-inflammatory activity of female Tregs. Our study emphasizes the urgent need for sex-stratified clinical and preclinical analyses.

Dataset Information

Sexual dimorphism in the fly brain.

Publications

Sexual dimorphism in the fly brain.

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