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Drosophila FoxP Mutants Are Deficient in Operant Self-Learning
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Abstract:
Intact function of the Forkhead Box P2 (FOXP2) gene is necessary for normal development of speech and language. This important role has recently been extended, first to other forms of vocal learning in animals and then also to other forms of motor learning. The homology in structure and in function among the FoxP gene members raises the possibility that the ancestral FoxP gene may have evolved as a crucial component of the neural circuitry mediating motor learning. Here we report that genetic manipulations of the single Drosophila orthologue, dFoxP, disrupt operant self-learning, a form of motor learning sharing several conceptually analogous features with language acquisition. Structural alterations of the dFoxP locus uncovered the role of dFoxP in operant self-learning and habit formation, as well as the dispensability of dFoxP for operant world-learning, in which no motor learning occurs. These manipulations also led to subtle alterations in the brain anatomy, including a reduced volume of the optic glomeruli. RNAi-mediated interference with dFoxP expression levels copied the behavioral phenotype of the mutant flies, even in the absence of mRNA degradation. Our results provide evidence that motor learning and language acquisition share a common ancestral trait still present in extant invertebrates, manifest in operant self-learning. This ‘deep’ homology probably traces back to before the split between vertebrate and invertebrate animals. Figure S2: Separating the genetic control groups still shows the RNAi effect in operant self-learning. Both genetic control lines show significant learning scores of 0.37 and above (t-tests against zero, elav/+: t = 2.26, p = 0.038; RNAi/+: t = 3.53, p = 0.004). In contrast, the flies from the strain in which the elav driver expressed the isoform B-specific RNAi construct in all neurons, fails to reach even half of the lowest control score with a PI of less than 0.17, which cannot be distinguished from a PI of zero (t-test against zero; t = 0.141, P = 0.166). Figure S3: Subtle morphological alterations in the brains of FoxP³⁹⁵⁵ mutants. a, Three-dimensional surface renderings of typical fly brains from wild type Canton S (a1) and FoxP³⁹⁵⁵ mutants (a2). In the online version, clicking on the reconstructions will activate the 3D features of the figure and allow for interactions with the object in space. The different neuropil areas can be selected in the pop-up menu. b, Quantitative volumetric analysis of eleven major neuropils (M – medulla, L – lobula, LP – lobula plate, MB – mushroom bodies, AL – antennal lobes, FB – fan-shaped body, OT – optic tubercle, EB – ellipsoid body, OG – optic glomeruli (purple in a), PB – protocerebral bridge, N – noduli) revealed a significant reduction in the volume of the optic glomeruli in FoxP³⁹⁵⁵ flies (Mann-Whitney U-Test, U = 2.0, p<0.002). The volume of the remaining neuropils (denoted PL – protocerebral lobes) did not differ significantly. Asterisk – significant difference with a Bonferroni-corrected level of p<0.004. Black stripes – median, boxes – 25–75% percentiles, whiskers – total range. Grey boxes indicate FoxP³⁹⁵⁵, white boxes Canton S. c, Principal Components Analysis of the volumetric data. Plotted are the factor loadings of the individual flies on the two first components. Colored bars indicate means and standard errors (PC). Factor loadings are significantly different between Canton S and Foxp³⁹⁵⁵ for PC1 (Mann-Whitney U-Test, U = 52.0, p<0.04), but fail to reach significance for PC2. Number of brains analyzed: 7 (Canton S) and 9 (Foxp³⁹⁵⁵). Figure S4: PCA on relative volume data with optic glomeruli excluded from the analysis. The general distribution of the individual fly brains remains roughly similar to the PCA on all data (Fig. 6), suggesting that the exclusion of the volume data from the optic glomeruli does not drastically alter the general picture of anatomical differences between the mutant and wild type flies also outside of the optic glomeruli. However, the ANOVA on the differences between the two groups now fails to reach significance, emphasizing the importance of the volume difference we found in the optic glomeruli.
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Keyword:
570 Biowissenschaften; 610 Medizin; Biologie; ddc:570; ddc:610
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URL: http://figshare.com/articles/_Drosophila_FoxP_Mutants_Are_Deficient_in_Operant_Self_Learning/1084271
https://epub.uni-regensburg.de/31538/3/Figure_S4.eps
https://epub.uni-regensburg.de/31538/2/Figure_S3.pdf
https://epub.uni-regensburg.de/31538/1/Figure_S2.eps
https://epub.uni-regensburg.de/31538/
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Drosophila FoxP Mutants Are Deficient in Operant Self-Learning
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