Inhibitory Circuit Maturation Shapes Sensory–Motor Integration During Song Learning

Vallentin D, Kosche G, Lipkind D, Long MA. Neural circuits. Inhibition protects acquired song segments during vocal learning in zebra finches. Science 2016;351(6270):267-271. doi: 10.1126/science.aad3023.

Background: Vocal imitation learning requires that sensory information from a tutor be integrated into the motor circuits responsible for song production. In zebra finches, this process involves thescain forebrain nucleus HVC, which connects auditory inputs with premotor output neurons. While juveniles show strong tutor song–evoked activity in HVC during learning, the mechanisms by which this responsiveness changes with development and learning remain unclear.

Hypothesis: This study hypothesized that inhibitory synaptic activity within the HVC circuit strengthens with learning and functions to suppress sensory responses in premotor neurons for song elements that have already been mastered.

Methods: The authors performed electrophysiological recordings in awake juvenile and adult male zebra finches. Birds were reared under controlled tutoring conditions, and recordings targeted HVC neurons projecting to the robust nucleus of the arcopallium. Sharp intracellular, juxtacellular and two-photon targeted whole-cell recordings were obtained using a customized moveable-objective two-photon microscope, a laser tuned to 800 nm, and images were captured with ScanImage. The authors used an oil-based pressure injection system, motorized micromanipulator and an amplifier for voltage-clamp recordings. In some adults, a GABA_A antagonist (gabazine) was locally applied to test the role of inhibition.

Results: Tutor song playback evoked precise spiking in HVC premotor neurons of juveniles but not adults. Blocking inhibition reinstated these responses in adults, revealing that synaptic inhibition suppresses sensory inputs after learning. The strength, frequency and temporal precision of inhibitory currents correlated with each bird’s similarity to the tutor song rather than age. During artificial tutoring, inhibition selectively targeted learned syllables, while unlearned segments remained less inhibited.

Conclusions: These findings show that learning-dependent inhibition in HVC protects acquired song elements from further modification, thereby enabling sequential mastery of complex motor sequences.