Contributions of Tutor and Bird’s Own Song Experience to Neural Selectivity in the Songbird Anterior Forebrain

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Abstract
Auditory neurons of the anterior forebrain (AF) of zebra finches become selective for song during song learning. In adults, these neurons respond more to the bird’s own song (BOS) than to the songs of other zebra finches (conspecifics) or BOS played in reverse. In contrast, AF neurons from young birds (30 d) respond equally well to all song stimuli. AF selectivity develops rapidly during song learning, appearing in 60-d-old birds. At this age, many neurons also respond equally well to BOS and tutor song. These similar neural responses to BOS and tutor song might reflect contributions from both song experiences to selectivity, because auditory experiences of both BOS and tutor song are essential for normal song learning. Alternatively, they may simply result from acoustic similarities between BOS and tutor song. Understanding which experience shapes selectivity could elucidate the function of song-selective AF neurons. To minimize acoustic similarity between BOS and tutor song, we induced juvenile birds to produce abnormal song by denervating the syrinx, the avian vocal organ, before song onset. We recorded single neurons extracellularly in the AF at 60 d, after birds had had substantial experience of both the abnormal BOS (tsBOS) and tutor song. Some neurons preferred the unique tsBOS over the tutor song, clearly indicating a role for BOS experience in shaping neural selectivity. In addition, a sizable proportion of neurons responded equally well to tsBOS and tutor song, despite their acoustic dissimilarity. These neurons were not simply immature, because they were selective for tsBOS and tutor song relative to conspecific and reverse song. Furthermore, their similar responses to tsBOS and tutor song could not be attributed to residual acoustic similarities between the two stimuli, as measured by several song analyses. The neural sensitivity to two very different songs suggests that single AF neurons may be shaped by both BOS and tutor song experience.