Thalamic maintenance of a complex sequential learned behavior: birdsong

Performing learned behaviors requires animals to produce precisely timed motor sequences. Birdsong is an excellent natural example of a complex, learned and precisely timed behavior. In the zebra finch we asked how thalamocortical input contributes to song dynamics. Birdsong is controlled by a brainstem-thalamocortical feedback loop. The premotor cortical region HVC (proper name) contains projection neurons that produce precisely timed, highly reliable and ultra-sparse spike burst sequences that underlie song dynamics. The origin of these bursts is debated. One model posits that bursts are generated locally in HVC through a synaptic chain mechanism. Alternatively, the thalamic nucleus Uveaformis (Uva), could drive HVC bursts as part of the brainstem-thalamocortical distributed network. Despite its importance, single unit recordings from Uva during singing have never been reported and consequently, the exact circuit-level function of this nucleus is unknown. We developed a lightweight (~1 g) microdrive for juxtacellular recordings and with it performed the very first extracellular single unit recordings in Uva during song. Recordings revealed HVC-projecting Uva neurons contain timing information during the song, but compared to HVC neurons, fire densely in time and are much less reliable. Computational models of Uva-driven HVC neurons estimated that a high degree of synaptic convergence is needed from Uva to HVC to overcome the inconsistency of Uva firing patterns. However, traced axon terminals of single Uva neurons showed low convergence within HVC such that each HVC neuron receives input from only 2-3 Uva neurons. These results suggest that Uva maintains sequential cortical activity during song but does not provide unambiguous timing information. Our observations are consistent with a model in which the brainstem-thalamocortical feedback loop acts at the syllable timescale (~100 ms) and does not support a model in which the brainstem-thalamocortical feedback loop acts at fast timescale (~10 ms) to generate sequences within cortex.