Cortical–basal ganglia circuits have a critical role in motor control and motor learning1. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia–forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song2,3,4,5. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song6,7. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Scientific Reports Open Access 04 August 2022
Scientific Reports Open Access 17 November 2021
Nature Communications Open Access 11 May 2021
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Graybiel, A. M., Aosaki, T., Flaherty, A. W. & Kimura, M. The basal ganglia and adaptive motor control. Science 265, 1826–1831 (1994)
Bottjer, S. W., Miesner, E. A. & Arnold, A. P. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901–903 (1984)
Scharff, C. & Nottebohm, F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11, 2896–2913 (1991)
Brainard, M. S. & Doupe, A. J. Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations. Nature 404, 762–766 (2000)
Williams, H. & Mehta, N. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J. Neurobiol. 39, 14–28 (1999)
Tchernichovski, O., Mitra, P. P., Lints, T. & Nottebohm, F. Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291, 2564–2569 (2001)
Williams, H., Cynx, J. & Nottebohm, F. Timbre control in zebra finch (Taeniopygia guttata) song syllables. J. Comp. Psychol. 103, 366–380 (1989)
Nottebohm, F., Stokes, T. M. & Leonard, C. M. Central control of song in the canary. J. Comp. Neurol. 165, 457–486 (1976)
Perkel, D. J. in Behavioral Neurobiology of Birdsong (eds Zeigler, H. P. & Marler, P.) 736–748 (New York Academy of Sciences, New York, 2004)
Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning. II. Temporal hierarchies and the learning of song sequence. J. Neurophys. 84, 1224–1239 (2000)
Doya, K. & Sejnowski, T. J. in The New Cognitive Neurosciences (ed. Gazzaniga, M. S.) 469–482 (MIT Press, Cambridge, Massachusetts, 2000)
Hessler, N. A. & Doupe, A. J. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci. 2, 209–211 (1999)
Hessler, N. A. & Doupe, A. J. Singing-related neural activity in a dorsal forebrain–basal ganglia circuit of adult zebra finches. J. Neurosci. 19, 10461–10481 (1999)
Vu, E. T., Mazurek, M. E. & Kuo, Y. C. Identification of a forebrain motor programming network for the learned song of zebra finches. J. Neurosci. 14, 6924–6934 (1994)
Vicario, D. S. & Simpson, H. B. Electrical stimulation in forebrain nuclei elicits learned vocal patterns in songbirds. J. Neurophys. 73, 2602–2607 (1995)
Brumm, H. & Todt, D. Male–male vocal interactions and the adjustment of song amplitude in a territorial bird. Anim. Behav. 67, 281–286 (2004)
Yu, A. C. & Margoliash, D. Temporal hierarchical control of singing in birds. Science 273, 1871–1875 (1996)
Johnson, F., Sablan, M. M. & Bottjer, S. W. Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J. Comp. Neurol. 358, 260–278 (1995)
Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000)
Jarvis, E. D., Scharff, C., Grossman, M. R., Ramos, J. A. & Nottebohm, F. For whom the bird sings: context-dependent gene expression. Neuron 21, 775–788 (1998)
Hikosaka, O., Nakamura, K., Sakai, K. & Nakahara, H. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217–222 (2002)
Miller, E. K. The prefrontal cortex and cognitive control. Nature Rev. Neurosci. 1, 59–65 (2000)
Troyer, T. W. & Bottjer, S. W. Birdsong: models and mechanisms. Curr. Opin. Neurobiol. 11, 721–726 (2001)
Mooney, R. & Konishi, M. Two distinct inputs to an avian song nucleus activate different glutamate receptor subtypes on individual neurons. Proc. Natl Acad. Sci. USA 88, 4075–4079 (1991)
Kittelberger, J. M. & Mooney, R. Lesions of an avian forebrain nucleus that disrupt song development alter synaptic connectivity and transmission in the vocal premotor pathway. J. Neurosci. 19, 9385–9398 (1999)
Stark, L. L. & Perkel, D. J. Two-stage input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch. J. Neurosci. 19, 9107–9116 (1999)
Komatsu, H. & Wurtz, R. H. Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J. Neurophys. 62, 31–47 (1989)
Tanaka, M. & Lisberger, S. G. Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex. Nature 409, 191–194 (2001)
Canales, J. J. & Graybiel, A. M. A measure of striatal function predicts motor stereotypy. Nature Neurosci. 3, 377–383 (2000)
Matsumoto, N., Hanakawa, T., Maki, S., Graybiel, A. M. & Kimura, M. Nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J. Neurophys. 82, 978–997 (1999)
We thank N. Hessler for a portion of the data in Fig. 3e. We thank A. Basbaum, S. Lisberger, J. Sakata and B. Wright for helpful comments on this manuscript and A. Arteseros and K. McManaway for technical assistance. This work was supported by an HHMI Predoctoral Fellowship (M.H.K.), the MacArthur Foundation, the Steven and Michele Kirsch Foundation, NARSAD and NIH (A.J.D.), and the HHMI Biomedical Research Support Program grant, the McKnight Foundation, the Klingenstein Fund, a Searle Scholars Award and NIH (M.S.B.).
The authors declare that they have no competing financial interests.
This figure provides additional information for how the latency between the application of a stimulus and the onset of a change in syllable structure was measured. Latency measurements could be complicated because the effects of stimulation at a given site could be specific to a subset of syllables. (GIF 46 kb)
This figure shows a correlation between the magnitude of changes in LMAN variability and the magnitude of changes in song variability. (GIF 36 kb)
Summary of the effects of stimulation in LMAN for each syllable tested in 5 birds. (DOC 72 kb)
Summary of the effects of LMAN stimulation for each bird by site. Stimulation evoked significant changes in syllable structure in 18/20 sites in LMAN of 5 birds. (DOC 34 kb)
Summary of the effects of differential activation of LMAN neurons at a particular site. (DOC 51 kb)
About this article
Cite this article
Kao, M., Doupe, A. & Brainard, M. Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song. Nature 433, 638–643 (2005). https://doi.org/10.1038/nature03127
Scientific Reports (2022)
Scientific Reports (2021)
Nature Communications (2021)
Scientific Reports (2021)