Data from: Drosophila FoxP mutants are deficient in operant self-learning

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.

叉头框P2（Forkhead Box P2, FOXP2）基因的完整功能，对于语音与语言的正常发育不可或缺。该基因的重要生理功能近来得到了拓展：其首先被证实参与动物的其他发声学习过程，后续又被发现与多种运动学习形式密切相关。FoxP基因家族成员在结构与功能上的同源性，提示祖先FoxP基因可能作为介导运动学习的神经环路关键组分演化而来。本研究表明，对果蝇（Drosophila）的单一直系同源基因dFoxP进行遗传操作，会破坏操作性自我学习——这是一类运动学习形式，其若干概念层面的特征与语言习得具有相似性。对dFoxP基因座的结构改造，不仅揭示了dFoxP在操作性自我学习与习惯形成中的调控作用，还证实其对于操作性环境学习并非必需——后者并不涉及运动学习过程。这类遗传操作还会引发脑部解剖结构的细微改变，包括视神经小球体积的缩小。通过RNA干扰（RNAi）介导的dFoxP表达水平调控，即便在不发生mRNA降解的情况下，也可复制突变果蝇的行为表型。本研究结果提供了有力证据，表明运动学习与语言习得共享一类可追溯至古老祖先的共同性状，这一性状在现存无脊椎动物中以操作性自我学习的形式得以保留。这类“深度同源性”很可能可以追溯至脊椎动物与无脊椎动物分化之前的演化阶段。