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The Journal of Neuroscience, September 14, 2005, 25(37):8543-8554; doi:10.1523/JNEUROSCI.1668-05.2005

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Behavioral/Systems/Cognitive
Brainstem and Forebrain Contributions to the Generation of Learned Motor Behaviors for Song

Robin C. Ashmore,1 J. Martin Wild,3 and Marc F. Schmidt1,2

1Neuroscience Graduate Group and 2Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104, and 3Department of Anatomy, Faculty of Medical and Health Sciences, University of Auckland, PB 92019 Auckland, New Zealand

Brainstem nuclei have well established roles in generating nonlearned rhythmic behaviors or as output pathways for more complex, forebrain-generated behaviors. However, the role of the brainstem in providing information to the forebrain that is used to initiate or assist in the control of complex behaviors is poorly understood. In this study, we used electrical microstimulation in select nuclei of the avian song system combined with recordings of acoustic and respiratory output to examine how forebrain and brainstem nuclei interact in the generation of learned vocal motor sequences. We found that brief stimulation in the forebrain nuclei HVC (used as a proper name) and RA (robust nucleus of the arcopallium) caused a short-latency truncation of ongoing song syllables, which ultimately led to a cessation of the ongoing motor sequence. Stimulation within the brainstem inspiratory-related nucleus paraambigualis, which receives input from RA and projects back to HVC via the thalamus, caused syllable truncations and interruptions similar to those observed in HVC and RA. In contrast, stimulation in the tracheosyringal portion of the hypoglossal nucleus, which innervates the syrinx (the avian vocal organ) but possesses no known projections back into the song system, did not cause any significant changes in the song motor pattern. These findings suggest that perturbation of premotor activity in any nucleus within the recurrent song system motor network will disrupt the ongoing song motor sequence. Given the anatomical organization of this network, our results are consistent with a model in which the brainstem respiratory nuclei form an integral part of the song motor programming network by providing timing signals to song control nuclei in the forebrain.

Key words: brainstem; respiration; vocalization; motor control; birdsong; timing

Received April 27, 2005; revised July 29, 2005; accepted July 31, 2005.




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