Neural FoxP2 and FoxP1 expression in the budgerigar, an avian species with adult vocal learning

Abstract

Vocal learning underlies acquisition of both language in humans and vocal signals in some avian taxa. These bird groups and humans exhibit convergent developmental phases and associated brain pathways for vocal communication. The transcription factor FoxP2 plays critical roles in vocal learning in humans and songbirds. Another member of the forkhead box gene family, FoxP1 also shows high expression in brain areas involved in vocal learning and production. Here, we investigate FoxP2 and FoxP1 mRNA and protein in adult male budgerigars (Melopsittacus undulatus), a parrot species that exhibits vocal learning as both juveniles and adults. To examine these molecules in adult vocal learners, we compared their expression patterns in the budgerigar striatal nucleus involved in vocal learning, magnocellular nucleus of the medial striatum (MMSt), across birds with different vocal states, such as vocalizing to a female (directed), vocalizing alone (undirected), and non-vocalizing. We found that both FoxP2 mRNA and protein expressions were consistently lower in MMSt than in the adjacent striatum regardless of the vocal states, whereas previous work has shown that songbirds exhibit downregulation in the homologous region, Area X, only after singing alone. In contrast, FoxP1 levels were high in MMSt compared to the adjacent striatum in all groups. Taken together these results strengthen the general hypothesis that FoxP2 and FoxP1 have specialized expression in vocal nuclei across a range of taxa, and suggest that the adult vocal plasticity seen in budgerigars may be a product of persistent down-regulation of FoxP2 in MMSt.

Understanding Language from a Genomic Perspective

“…Although zebra finch vocal learning is restricted to juveniles, species like the budgerigar exhibit vocal plasticity in adulthood. In adult male budgerigars, FoxP2 levels within the striatal song nucleus (equivalent to Area X) are relatively low and are not modulated by singing, whether or not the song is directed to a female (62,197).…”

Social calls provide novel insights into the evolution of vocal learning

“…These similarities in brain mechanisms have helped propel research on song learning in birds. While fewer studies have examined mechanisms of call learning, there is evidence that some key genes, particularly FoxP2 , play similar roles in promoting song and call learning in birds (Hara et al, 2015; Whitney et al, 2015). Moreover, there is evidence that the song control pathway in the brain, which controls song production, also controls the vocal production of unlearned calls (Ter Maat et al, 2014), although, to our knowledge, no studies have yet examined the role of these regions in the production of learned calls in species that learn both calls and song.…”

Are northern mockingbirds classic open‐ended song learners?

“…One hypothesis based on a budgerigar study by Hara et al. (2015) is that downregulation of the FoxP2 gene in adults results in greater neuronal plasticity within a key brain region associated with vocal learning. Another hypothesis focused at the cellular level posits that the amount of neural plasticity during birdsong development is controlled by the amount of “perineuronal nets” of proteoglycans around various song control regions of the brain (Balmer, Carels, Frisch, & Nick, 2009; Cornez et al., 2017).…”