Intrinsic neuronal properties represent song and error in zebra finch vocal learning

Neurons regulate their intrinsic physiological properties, which could influence network properties and contribute to behavioral plasticity. Recording from adult zebra finch brain slices we show that within each bird basal ganglia Area X–projecting (HVC X ) neurons share similar spike waveform morphology and timing of spike trains, with modeling indicating similar magnitudes of five principal ion currents. These properties vary among birds in lawful relation to acoustic similarity of the birds’ songs, with adult sibling pairs (same songs) sharing similar waveforms and spiking characteristics. The properties are maintained dynamically: HVC X within juveniles learning to sing show variable properties, whereas the uniformity rapidly degrades within hours in adults singing while exposed to abnormal (delayed) auditory feedback. Thus, within individual birds the population of current magnitudes covary over the arc of development, while rapidly responding to changes in feedback (in adults). This identifies network interactions with intrinsic properties that affect information storage and processing of learned vocalizations. The regulation of cellular neuronal properties distinct from synaptic plasticity has been proposed as a mechanism of functional network organization. Here, the authors show that the magnitude of five ion currents in basal ganglia projection song system forebrain neurons covary across life, rapidly and dynamically relating to learned features of individual zebra finches’ songs.