Auditory Plasticity in a Basal Ganglia-Forebrain Pathway during Decrystallization of Adult Birdsong

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Abstract
Adult male zebra finches maintain highly stable songs via auditory feedback. Prolonged exposure to distorted feedback may cause this stable (i.e., “crystallized”) song to change its pattern, a process known as decrystallization. In the songbird, the telencephalic nucleus LMAN (lateral magnocellular nucleus of anterior nidopallium) is necessary for feedback-dependent song decrystallization, although whether and how electrophysiological properties of LMAN neurons change during decrystallization is unknown. In normal adult zebra finches, LMAN neurons exhibit highly selective responses to auditory presentation of the bird's own song (BOS), possibly providing a permanent referent for song maintenance. If so, LMAN neurons should maintain selectivity for the originally crystallized BOS after exposure to distorted feedback and during decrystallization. Alternatively, LMAN auditory selectivity in the adult may change during decrystallization. To distinguish between these possibilities, we sectioned the vocal nerve in adult male zebra finches, which spectrally distorted the birds' songs. Over the course of several weeks, experience of distorted feedback caused the song to decrystallize in a subset of birds. At various times after nerve section, electrophysiological recordings made under anesthesia revealed that auditory selectivity in LMAN could shift to the spectrally distorted song. Such auditory plasticity could be detected during the second week after nerve section, before the time birds typically decrystallized their songs. Moreover, all birds that underwent decrystallization at later times always manifested auditory plasticity in LMAN. To our knowledge, the present findings afford the first example of an electrophysiological correlate of song decrystallization.