Zenk expression in auditory regions changes with breeding condition in male Black-capped chickadees (Poecile atricapillus)

Black-capped chickadees (Poecile atricapillus) produce different vocalizations at different times of year: the fee-bee song is produced by males primarily in spring, whereas the chick-a-dee call is produced year-round but most frequently in the fall and winter. We wanted to determine if neural response to playback in auditory regions of the songbird brain varied with season in parallel to production. We captured adult male black-capped chickadees from the wild in either breeding condition or non-breeding condition and within 24-48 h of bringing them into the laboratory setting, played them recordings of either conspecific vocalizations (fee-bee songs or chick-a-dee calls), heterospecific vocalizations (Song Sparrow, Melospiza melodia, song), or silence. We then measured ZENK protein immunoreactivity (Zenk-ir) in caudomedial nidopallium (NCM) and caudomedial mesopallium (CMM), two regions important for perception of conspecific vocalizations. We found that, overall, non-breeding birds had greater Zenk-ir than breeding birds. In addition, we found that birds in non-breeding condition had significantly greater Zenk-ir to heterospecific song than birds in breeding condition, but this difference was not seen in birds that heard conspecific songs or calls. Finally, in NCMd chickadees had greater response to playback of conspecific vocalizations (when combining song and call groups) than playback of heterospecific vocalizations but only while in breeding condition. Our results qualify the claim that Zenk-ir is biased toward conspecific vocalizations, and indicate that specificity of neural response varies with season. Variation could be a result of increased production and perceptual demand in spring, or hormonal changes in breeding birds, possibly because chickadees display vocal plasticity in chick-a-dee calls in the fall, requiring a degree of neural plasticity across seasons.