Covert skill learning in a cortical-basal ganglia circuit
- PMID: 22699618
- PMCID: PMC3377745
- DOI: 10.1038/nature11078
Covert skill learning in a cortical-basal ganglia circuit
Abstract
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 learning; 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 repertoire. Here we show that the anterior forebrain pathway (AFP), a cortical-basal ganglia circuit, 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.
Figures




References
-
- Hikosaka O, Nakamura K, Sakai K, Nakahara H. Central mechanisms of motor skill learning. Curr Opin Neurobiol. 2002;12:217–22. - PubMed
-
- Houk JC, Adams JL, Barto AG. In: Models of Information Processing in the Basal Ganglia. Houk JC, Davis JL, Beiser DG, editors. MIT Press; Cambridge, Massachusetts: 1995. pp. 249–270.
-
- Suri RE, Schultz W. A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience. 1999;91:871–890. - PubMed
-
- Mooney R. Neural mechanisms for learned birdsong. Learn Mem. 2009;16:655–669. - PubMed
-
- Tumer EC, Brainard MS. Performance variability enables adaptive plasticity of ‘crystallized’ adult birdsong. Nature. 2007;450:1240–1244. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources
Other Literature Sources
Miscellaneous