Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning

Behavioural learning depends on the brain's capacity to respond to instructive experience and is often enhanced during a juvenile sensitive period. How instructive experience acts on the juvenile brain to trigger behavioural learning remains unknown. In vitro studies show that forms of synaptic strengthening thought to underlie learning are accompanied by increased stability, number and size of dendritic spines, the major site of excitatory synaptic transmission in the vertebrate brain1–7. In vivo imaging studies in sensory cortical regions reveal that these structural features can be affected by disrupting sensory experience and that spine turnover is elevated during sensitive periods for sensory map formation8–12. These observations support two hypotheses: 1) the increased capacity for behavioural learning during a sensitive period is associated with enhanced spine dynamics on sensorimotor neurons important to the learned behaviour; 2) instructive experience rapidly stabilizes and strengthens these dynamic spines. Here we tested these hypotheses using two-photon in vivo imaging to measure spine dynamics in zebra finches, which learn to sing by imitating a tutor song during a juvenile sensitive period13,14. Spine dynamics were measured in the forebrain nucleus HVC, the proximal site where auditory information merges with an explicit song motor representation15–19, immediately before and after juvenile finches first experienced tutor song20. Higher levels of spine turnover prior to tutoring correlated with a greater capacity for subsequent song imitation. In juveniles with high levels of spine turnover, hearing a tutor song led to the rapid (~24h) stabilization, accumulation and enlargement of dendritic spines in HVC. Moreover, in vivo intracellular recordings made immediately before and after the first day of tutoring revealed robust enhancement of synaptic activity in HVC. These findings suggest behavioural learning results when instructive experience is able to rapidly stabilize and strengthen synapses on sensorimotor neurons important to the control of the learned behaviour.