Covert skill learning in a cortical-basal ganglia circuit.
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.
W. M. Keck Center for Integrative Neuroscience, Department of Physiology, University of California, San Francisco, California 94143, USA. jcharles@phy.ucsf.edu
Jonathan D
JD
Charlesworth
Timothy L
TL
Warren
Michael S
MS
Brainard
D015763:2-Amino-5-phosphonovalerate / Q000494:pharmacology; D000818:Animals; D001479:Basal Ganglia / Q000187:drug effects / Q000502:physiology*; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D046369:Finches / Q000033:anatomy & histology / Q000502:physiology*; D007858:Learning / Q000187:drug effects / Q000502:physiology*; D008297:Male; D016548:Prosencephalon / Q000502:physiology; D016194:Receptors, N-Methyl-D-Aspartate / Q000037:antagonists & inhibitors; D014828:Vocalization, Animal / Q000187:drug effects / Q000502:physiology*
D018691:Excitatory Amino Acid Antagonists; D016194:Receptors, N-Methyl-D-Aspartate; D015763:2-Amino-5-phosphonovalerate