Specialized Motor-Driven dusp1 Expression in the Song Systems of Multiple Lineages of Vocal Learning Birds

Abstract

Mechanisms for the evolution of convergent behavioral traits are largely unknown. Vocal learning is one such trait that evolved multiple times and is necessary in humans for the acquisition of spoken language. Among birds, vocal learning is evolved in songbirds, parrots, and hummingbirds. Each time similar forebrain song nuclei specialized for vocal learning and production have evolved. This finding led to the hypothesis that the behavioral and neuroanatomical convergences for vocal learning could be associated with molecular convergence. We previously found that the neural activity-induced gene dual specificity phosphatase 1 (dusp1) was up-regulated in non-vocal circuits, specifically in sensory-input neurons of the thalamus and telencephalon; however, dusp1 was not up-regulated in higher order sensory neurons or motor circuits. Here we show that song motor nuclei are an exception to this pattern. The song nuclei of species from all known vocal learning avian lineages showed motor-driven up-regulation of dusp1 expression induced by singing. There was no detectable motor-driven dusp1 expression throughout the rest of the forebrain after non-vocal motor performance. This pattern contrasts with expression of the commonly studied activity-induced gene egr1, which shows motor-driven expression in song nuclei induced by singing, but also motor-driven expression in adjacent brain regions after non-vocal motor behaviors. In the vocal non-learning avian species, we found no detectable vocalizing-driven dusp1 expression in the forebrain. These findings suggest that independent evolutions of neural systems for vocal learning were accompanied by selection for specialized motor-driven expression of the dusp1 gene in those circuits. This specialized expression of dusp1 could potentially lead to differential regulation of dusp1-modulated molecular cascades in vocal learning circuits.

Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns

“…However, we noted that in many of our and other previous studies, the induced expression patterns of the activity-dependent genes (EGR1, C-FOS, C-JUN, ARC, BDNF, and DUSP1) do not conform to the lamina-defined boundaries (Mello et al, 1992;Jarvis and Nottebohm, 1997;Jarvis et al, 1998;Velho et al, 2005;Wada et al, 2006;Feenders et al, 2008;Hara et al, 2009;Horita et al, 2010Horita et al, , 2012. These genes are upregulated in subsets of cell types in different brain regions when the animals process specific sensory stimuli or perform repeated motor behaviors; the genes can thus can be used to map physiological activation of different cell types within functionally connected neural systems (Feenders et al, 2008;Hara et al, 2009;Horita et al, 2010Horita et al, , 2012. EGR1, C-FOS, C-JUN, and ARC are all inducible in pallial and striatal cells except the primary sensory neurons (particularly for EGR1; (Mello and Clayton, 1995;Wada et al, 2006;Feenders et al, 2008).…”

“…map kinase phosphatase 1 [mkp1]), and PPAPDC1A enzymes Horita et al, 2010Horita et al, , 2012; and a diverse set of membrane and cytoplasmic genes, including ARPP16 (this study), TMEM100 (this study), ARC, CADPS2, and S100B (Wada et al, 2006;Lovell et al, 2008) (Table 1). Among these genes, BDNF, EGR1, C-FOS, C-JUN, DUSP1, and ARC are activity regulated in the brain by sensory and motor behaviors (Mello et al, 1992;Jarvis and Nottebohm, 1997;Kimpo and Doupe, 1997;Wada et al, 2006;Horita et al, 2010).…”

“…All animals were laboratory raised except the hummingbirds, which were captured from wild populations in Santa Theresa, Espirito Santo, Brazil (sombre hummingbird and rufous-breasted hermit) and in Riverside, California (Anna's hummingbird) Feenders et al, 2008), and the garden warblers which were caught on Helgoland and around Oldenburg, Germany (Mouritsen et al, 2005). These wild-caught birds and some of the brain sections from the other species are from animals collected in our prior studies Wada et al, 2004;Mouritsen et al, 2005;Feenders et al, 2008;Horita et al, 2010Horita et al, , 2012Kubikova et al, 2010 Because sensory stimuli or behavioral performance are associated with changes in expression of activity-dependent genes in the associated brain circuits, to assess basal expression patterns we measured gene expression in the brains of animals that were in silent control conditions, either with lights off or on after an overnight period of silence. To examine stimulus and behaviorally regulated patterns of the activity-dependent genes (BDNF, EGR1, C-FOS, C-JUN, ARC, and DUSP1), we used brain sections from animals that had undergone controlled behavioral experiments in our prior studies.…”

Rudimentary substrates for vocal learning in a suboscine

“…However, the phoebe's RA-like region is different from that of oscines because of the lack of expression of certain genes (that is, GRM2, GRIN2A, PV, Egr1, and dusp1 (ref. 19)) that are found expressed in the oscine RA; because there is no direct projection from it to the tracheosyringeal hypoglossal nucleus; and the lack of connections to the other forebrain regions that are important for vocal learning.…”

“…1a). While all oscines are thought to have vocal learning, most suboscines are thought to lack this learning plasticity and lack the discrete forebrain nuclei that are associated with vocal learning in oscines [18][19][20][21] . However, at least a few suboscine species, such as the three-wattled bellbird (Procnias tricarunculata, of Cotingidae) and the long-tailed manakin (Chiroxiphia linearis, of Pipridae), show vocal matching or song geographic variation [22][23][24] , suggesting that vocal learning may have evolved in these groups as well, but the underlying neural substrates remain unknown.…”