Convergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners.
Journal Article (Journal Article)
Only a few distantly related mammals and birds have the trait of complex vocal learning, which is the ability to imitate novel sounds. This ability is critical for speech acquisition and production in humans, and is attributed to specialized forebrain vocal control circuits that have several unique connections relative to adjacent brain circuits. As a result, it has been hypothesized that there could exist convergent changes in genes involved in neural connectivity of vocal learning circuits. In support of this hypothesis, expanding on our related study (Pfenning et al. [2014] Science 346: 1256846), here we show that the forebrain part of this circuit that makes a relatively rare direct connection to brainstem vocal motor neurons in independent lineages of vocal learning birds (songbird, parrot, and hummingbird) has specialized regulation of axon guidance genes from the SLIT-ROBO molecular pathway. The SLIT1 ligand was differentially downregulated in the motor song output nucleus that makes the direct projection, whereas its receptor ROBO1 was developmentally upregulated during critical periods for vocal learning. Vocal nonlearning bird species and male mice, which have much more limited vocal plasticity and associated circuits, did not show comparable specialized regulation of SLIT-ROBO genes in their nonvocal motor cortical regions. These findings are consistent with SLIT and ROBO gene dysfunctions associated with autism, dyslexia, and speech sound language disorders and suggest that convergent evolution of vocal learning was associated with convergent changes in the SLIT-ROBO axon guidance pathway.
Full Text
- Published version (via Digital Object Identifier)
- Pubmed Central version
- Open Access Copy from Duke
- Link to Item
Duke Authors
Cited Authors
- Wang, R; Chen, C-C; Hara, E; Rivas, MV; Roulhac, PL; Howard, JT; Chakraborty, M; Audet, J-N; Jarvis, ED
Published Date
- April 15, 2015
Published In
Volume / Issue
- 523 / 6
Start / End Page
- 892 - 906
PubMed ID
- 25424606
Pubmed Central ID
- PMC4329046
Electronic International Standard Serial Number (EISSN)
- 1096-9861
Digital Object Identifier (DOI)
- 10.1002/cne.23719
Language
- eng
Conference Location
- United States