Context-specific habituation of the zenk gene response to song in adult zebra finches

Zebra finches show a multifaceted response to playback of tape-recorded birdsong. A novel song induces an overt listening behavior, accompanied by a distinct electrophysiological signature and a wave of gene expression in the auditory telencephalon. With repetition of the same song these responses all habituate; habituation can persist for a day or more and is specific for the repeated song. This habituation is a form of selective memory. Here we describe four experiments to probe the nature of the information stored in that memory, using habituation of the genomic response as a physiological assay for stimulus recognition. Adult male zebra finches (awake and unrestrained) were exposed to repetitions of a test song to habituate the genomic response. The same song was then presented in one of four different contexts: (1) from a speaker on the opposite side of the cage; (2) at a reduced sound pressure level; (3) paired with constant illumination of colored lights next to the speaker; (4) paired with colored lights that were turned on and off in synchrony with each song bout. In all cases except the third, a "familiar" (habituated) song re-induced a new wave of gene expression in the auditory telencephalon when presented in the new context. These results reveal that memory for a specific song, as indicated by the initial gene habituation, incorporates more than just an acoustic description of the song. We suggest that habituation in the auditory telencephalon is controlled in part by an extrinsic system that allows detection of synchronous activity in different sensory or representational modalities. (C) 2004 Elsevier Inc. All rights reserved.