Hierarchical Organization of Auditory Temporal Context Sensitivity

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Abstract
Some of the most complex auditory neurons known are contained in the songbird forebrain nucleus HVc. These neurons are highly sensitive to auditory temporal context: they respond strongly to the bird’s own song, but respond weakly or not at all when the sequence of the song syllables is altered. It is not known whether this property arises de novo in HVc or whether it is relayed from the properties of neurons in afferent nuclei. To address this issue, we recorded from neurons in both HVc and its afferent nuclei, collectively called field L. Experimental tests were designed to determine the degree of auditory context sensitivity in field L and HVc. Tests were also performed to compare the responses to individual syllables and syllable combinations to see whether these responses could account for the response seen to the entire song. Our results show a substantial increase in the auditory temporal context sensitivity between field L and HVc. Most field L neurons respond equally well both to normal song and to temporally manipulated versions of the same song. A few field L neurons show sensitivity to local temporal structure, such as the sequence of syllable pairs. In contrast, HVc neurons are highly dependent on the song’s local and global temporal structure. This shows that HVc neurons can integrate auditory context over periods much longer than neurons in field L and suggests that additional mechanisms are required to explain the marked sensitivity of HVc neurons to the temporal structure of the bird’s own song.