Drosophila FoxP Mutants Are Deficient in Operant Self-Learning

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.

FoxP expression identifies a Kenyon cell subtype in the honeybee mushroom bodies linking them to fruit fly αβc neurons

“…Recently, one type of KC, the αβ c neurons were shown to express the transcription factor dFoxP (DasGupta et al ., ). The dFoxP gene affects motor learning, decision‐making and courtship behaviour in Dm (DasGupta et al ., ; Lawton et al ., ; Mendoza et al ., ). Experimentally altered dFoxP levels in αβ c neurons decrease the speed of decision‐making in an olfactory discrimination learning task (DasGupta et al ., ).…”

Outcome learning, outcome expectations, and intentionality inDrosophila

“…It is also dispensable in classical odor intensity learning (Masek and Heisenberg 2008). The genes pkc and dFoxP are required in yawtorque learning but dispensable in the classical component of switch-mode learning (Brembs and Plendl 2008;Mendoza et al 2014). The gene "ignorant" is involved in classical and operant learning in different ways (Putz et al 2004).…”

Place memory retention in Drosophila

“…The rut and lat results add to our understanding of an apparently common set of short-term changes in memory between olfactory and place memory, which include a common function of the S6 kinase II, an atypical tribbles kinase, and the arouser EPS8L3 (Laferriere, Ostrowski, Guarnieri, & Zars, 2011;LaFerriere, Speichinger, et al, 2011;Putz, Bertolucci, Raabe, Zars, & Heisenberg, 2004). And, the recently identified role of the foxp transcription factor specifically in operant learning, as tested in a flight simulator, suggests another set of genes that could be important for operant place memory in the minutes range (Mendoza et al, 2014).…”