The climbing fiber input to the cerebellar cortex is thought to provide instructive signals that drive the induction of motor skill learning. We found that optogenetic activation of Purkinje cells, the sole output neurons of the cerebellar cortex, can also drive motor learning in mice. This dual control over the induction of learning by climbing fibers and Purkinje cells can expand the learning capacity of motor circuits.

Mechanisms underlying the learned vocal behavior of songbirds were studied by examining expression of the protein product of the immediate early gene c-fos (Fos) in zebra finches. Auditory stimuli including the bird's own song did not induce Fos in the song system. In contrast, the motor act of singing induced Fos in two song sensorimotor nuclei, HVc and RA. This induction was independent of auditory feedback, since it occurred in deafened birds that sang. Double-labeling studies demonstrated that only one of the two sets of projection neurons in HVc expressed singing-related Fos. The motor-driven induction of Fos identifies functionally distinct cell populations in a network for singing and may point to sites of cellular plasticity necessary for song maintenance.

Cerebellar climbing fiber activity encodes performance errors during many motor learning tasks, but the role of these error signals in learning has been controversial. We compared two motor learning paradigms that elicited equally robust putative error signals in the same climbing fibers: learned increases and decreases in the gain of the vestibulo-ocular reflex (VOR). During VOR-increase training, climbing fiber activity on one trial predicted changes in cerebellar output on the next trial, and optogenetic activation of climbing fibers to mimic their encoding of performance errors was sufficient to implant a motor memory. In contrast, during VOR-decrease training, there was no trial-by-trial correlation between climbing fiber activity and changes in cerebellar output, and climbing fiber activation did not induce VOR-decrease learning. Our data suggest that the ability of climbing fibers to induce plasticity can be dynamically gated in vivo, even under conditions where climbing fibers are robustly activated by performance errors.DOI: http://dx.doi.org/10.7554/eLife.02076.001

The timing of spikes can carry information, for instance, when the temporal pattern of firing across neurons results in correlated activity. However, in part because central synapses are unreliable, correlated activity has not been observed to propagate through multiple subsequent stages in neural circuits, although such propagation has frequently been used in theoretical models. Using simultaneous single-unit and multiunit recordings from two or three vocal control nuclei of songbirds, measurement of coherency and time delays, and manipulation of neural activity, we provide evidence here for preserved correlation of activity through multiple steps of the neural circuit for song, including a basal ganglia circuit and its target vocal motor pathway. This suggests that these pathways contain highly functionally interconnected neurons and represent a neural architecture that can preserve information about the timing of firing of groups of neurons. Because the interaction of these song pathways is critical to vocal learning, the preserved correlation of activity may be important to the learning and production of sequenced motor acts and could be a general feature of basal ganglia-cortical interaction.