We learn complex skills such as speech and dance through a gradual process of trial and error. Cortical-basal ganglia circuits have an important yet unresolved function in this trial-and-error skill learning1; influential ‘actor–critic’ models propose that basal ganglia circuits generate a variety of behaviours during training and learn to implement the successful behaviours in their repertoire2,3. Here we show that the anterior forebrain pathway (AFP), a cortical-basal ganglia circuit4, contributes to skill learning even when it does not contribute to such ‘exploratory’ variation in behavioural performance during training. Blocking the output of the AFP while training Bengalese finches to modify their songs prevented the gradual improvement that normally occurs in this complex skill during training. However, unblocking the output of the AFP after training caused an immediate transition from naive performance to excellent performance, indicating that the AFP covertly gained the ability to implement learned skill performance without contributing to skill practice. In contrast, inactivating the output nucleus of the AFP during training completely prevented learning, indicating that learning requires activity within the AFP during training. Our results suggest a revised model of skill learning: basal ganglia circuits can monitor the consequences of behavioural variation produced by other brain regions and then direct those brain regions to implement more successful behaviours. The ability of the AFP to identify successful performances generated by other brain regions indicates that basal ganglia circuits receive a detailed efference copy of premotor activity in those regions. The capacity of the AFP to implement successful performances that were initially produced by other brain regions indicates precise functional connections between basal ganglia circuits and the motor regions that directly control performance.
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Hikosaka, O., Nakamura, K., Sakai, K. & Nakahara, H. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217–222 (2002)
Houk, J. C., Adams, J. L. & Barto, A. G. in Models of Information Processing in the Basal Ganglia (eds Houk, J. C., Davis, J. L. & Beiser, D. G. ) 249–270 (MIT Press, 1995)
Suri, R. E. & Schultz, W. A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience 91, 871–890 (1999)
Mooney, R. Neural mechanisms for learned birdsong. Learn. Mem. 16, 655–669 (2009)
Tumer, E. C. & Brainard, M. S. Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong. Nature 450, 1240–1244 (2007)
Charlesworth, J. D., Tumer, E. C., Warren, T. L. & Brainard, M. S. Learning the microstructure of successful behavior. Nature Neurosci. 14, 373–380 (2011)
Sutton, R. S. & Barto, A. G. Reinforcement Learning: An Introduction (MIT Press, 1998)
Schultz, W., Dayan, P. & Montague, P. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997)
Reynolds, J. N., Hyland, B. I. & Wickens, J. R. A cellular mechanism of reward-related learning. Nature 413, 67–70 (2001)
Fee, M. S. & Goldberg, J. H. A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neuroscience 198, 152–170 (2011)
Fiete, I. R., Fee, M. S. & Seung, H. S. Model of birdsong learning based on gradient estimation by dynamic perturbation of neural conductances. J. Neurophysiol. 98, 2038–2057 (2007)
Doya, K. & Sejnowski, T. in The New Cognitive Neurosciences (ed. Gazzaniga, M. ) 469–482 (MIT Press, 2000)
Andalman, A. S. & Fee, M. S. A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors. Proc. Natl Acad. Sci. USA 106, 12518–12523 (2009)
Warren, T. L., Tumer, E. C., Charlesworth, J. D. & Brainard, M. S. Mechanisms and time course of vocal learning and consolidation in the adult songbird. J. Neurophysiol. 106, 1806–1821 (2011)
Olveczky, B. P., Andalman, A. S. & Fee, M. S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3, e153 (2005)
Hampton, C. M., Sakata, J. T. & Brainard, M. S. An avian basal ganglia-forebrain circuit contributes differentially to syllable versus sequence variability of adult Bengalese finch song. J. Neurophysiol. 101, 3235–3245 (2009)
Krupa, D. J., Thompson, J. K. & Thompson, R. F. Localization of a memory trace in the mammalian brain. Science 260, 989–991 (1993)
Atallah, H. E., Lopez-Paniagua, D., Rudy, J. W. & O’Reilly, R. C. Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nature Neurosci. 10, 126–131 (2007)
Balleine, B. W. & Ostlund, S. B. Still at the choice-point: action selection and initiation in instrumental conditioning. Ann. NY Acad. Sci. 1104, 147–171 (2007)
Crapse, T. B. & Sommer, M. A. Corollary discharge across the animal kingdom. Nature Rev. Neurosci. 9, 587–600 (2008)
Olveczky, B. P., Otchy, T. M., Goldberg, J. H., Aronov, D. & Fee, M. S. Changes in the neural control of a complex motor sequence during learning. J. Neurophysiol. 106, 386–397 (2011)
Sober, S. J., Wohlgemuth, M. J. & Brainard, M. S. Central contributions to acoustic variation in birdsong. J. Neurosci. 28, 10370–10379 (2008)
Leonardo, A. Experimental test of the birdsong error-correction model. Proc. Natl Acad. Sci. USA 101, 16935–16940 (2004)
Vates, G. E., Vicario, D. S. & Nottebohm, F. Reafferent thalamo-‘cortical’ loops in the song system of oscine songbirds. J. Comp. Neurol. 380, 275–290 (1997)
Goldberg, J. H. & Fee, M. S. A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds. Nature Neurosci. 15, 620–627 (2012)
Redgrave, P. & Gurney, K. The short-latency dopamine signal: a role in discovering novel actions? Nature Rev. Neurosci. 7, 967–975 (2006)
Turner, R. S. & Desmurget, M. Basal ganglia contributions to motor control: a vigorous tutor. Curr. Opin. Neurobiol. 20, 704–716 (2010)
Frank, M. J. Computational models of motivated action selection in corticostriatal circuits. Curr. Opin. Neurobiol. 21, 381–386 (2011)
We thank L. Frank, A. Doupe, M. Stryker and D. Mets for discussion and comments on the manuscript. This work was supported by National Institutes of Health grant NIDCD R01 and National Institute of Mental Health grant P50. J.D.C. and T.L.W. were supported by National Science Foundation graduate fellowships.
The authors declare no competing financial interests.
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Charlesworth, J., Warren, T. & Brainard, M. Covert skill learning in a cortical-basal ganglia circuit. Nature 486, 251–255 (2012). https://doi.org/10.1038/nature11078
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