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The Journal of Neuroscience, March 26, 2008, 28(13):3479-3489; doi:10.1523/JNEUROSCI.0177-08.2008

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Behavioral/Systems/Cognitive
Telencephalic Neurons Monosynaptically Link Brainstem and Forebrain Premotor Networks Necessary for Song

Todd F. Roberts,¹ Marguerita E. Klein,¹ M. Fabiana Kubke,² J. Martin Wild,² and Richard Mooney¹

¹Department of Neurobiology, Duke University Medical Center, Durham, North Carolina 27710, and ²Department of Anatomy, Faculty of Medical and Health Sciences, University of Auckland, Auckland 1142, New Zealand

Correspondence should be addressed to Richard Mooney, Department of Neurobiology, Box 3209, Duke University Medical Center, Durham, NC 27710. Email: mooney{at}neuro.duke.edu

Birdsong, like human speech, is a series of learned vocal gestures resulting from the coordination of vocal and respiratory brainstem networks under the control of the telencephalon. The song motor circuit includes premotor and motor cortical analogs, known as HVC (used as a proper name) and RA (the robust nucleus of the arcopallium), respectively. Previous studies showed that HVC projects to RA and that RA projection neurons (PNs) topographically innervate brainstem vocal-motor and respiratory networks. The idea that singing-related activity flows between HVC and RA in a strictly feedforward manner is a central component of all models of song production. In contrast to this prevailing view of song motor circuit organization, we show that RA sends a reciprocal projection directly to HVC. Lentiviral labeling of RA PN axons and transgene tagging of RA PN synaptic terminals reveal a direct projection from RA to HVC. Retrograde tracing from HVC demonstrates that this projection originates exclusively from neurons in dorsocaudal regions of RA. Using dual retrograde tracer injections, we further show that many of these RA_HVC neurons also innervate the brainstem nucleus retroambigualis, which is premotor to expiratory motoneurons, thereby identifying a population of RA PNs positioned to coordinate activity at higher and lower levels of the song motor circuit. In combination, our findings identify a previously unknown pathway that may enable a subset of RA neurons to provide song-related signals to the respiratory brainstem but also transmit a copy of this information to song patterning networks in HVC.

Key words: lentivirus; zebra finch; motor control; anterograde; synaptophysin; vocal learning; songbird; avian

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Received Feb. 27, 2007; revised Feb. 14, 2008; accepted Feb. 14, 2008.

Correspondence should be addressed to Richard Mooney, Department of Neurobiology, Box 3209, Duke University Medical Center, Durham, NC 27710. Email: mooney{at}neuro.duke.edu

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