Abstract
How the evolution of complex behavioral traits is associated with the emergence of novel brain pathways is largely unknown. Songbirds, like humans, learn vocalizations via tutor imitation and possess a specialized brain circuitry to support this behavior. In a comprehensive in situ hybridization effort, we show that the zebra finch vocal robust nucleus of the arcopallium (RA) shares numerous markers (e.g. SNCA, PVALB) with the adjacent dorsal intermediate arcopallium (AId), an avian analog of mammalian deep cortical layers with involvement in motor function. We also identify markers truly unique to RA and thus likely linked to modulation of vocal motor function (e.g. KCNC1, GABRE), including a subset of the known shared markers between RA and human laryngeal motor cortex (e.g. SLIT1, RTN4R, LINGO1, PLXNC1). The data provide novel insights into molecular features unique to vocal learning circuits, and lend support for the motor theory for vocal learning origin.
Highlights
May have convergently evolved across different vocal learning systems
To provide complete and precise definitions of the dorsal intermediate arcopallium (AId) and of RA (Fig. 1A), we mapped the expression of SCN3B in adult zebra finches using in situ hybridization
We investigated the expression of a large set of differential arcopallial markers in zebra finches in order to better define AId in a songbird, examine the molecular relationships between RA and AId and other arcopallial domains, and more precisely identify molecular features unique to the vocal motor system
Summary
May have convergently evolved across different vocal learning systems. Notably, an extensive examination of the brain expression patterns of shared RA and LMC markers has not yet been performed. While lesions to RA result in severe song deficits[5], birds show marked motor deficits including akinesia and immobility in large lesions that primarily include AId53 These observations are consistent with AId being involved in somatic motor c ontrol[33], though other studies suggest a role in vocal learning[54]. Our data provide substantial further support for a close molecular similarity between RA and AId, as well as a more in-depth definition of features unique to RA and the vocal control circuitry They suggest that AId may represent a subdivision of the arcopallium that existed prior to the emergence of vocal learning circuits in birds, and are consistent with the hypothesis that RA may have evolved as a specialization of AId
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