Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds

There is both extensive species-specificity and critical experience-dependence in the recognition of own species songs in many songbird species. For example, female zebra finches Taeniopygia guttata raised by their parents show behavioral preferences for the songs of the father over unfamiliar conspecific males and for unfamiliar songs of conspecifics over heterospecifics. Behavioral discrimination between different species’ songs is also displayed by females raised without exposure to any male songs but it is diminished in females raised by heterospecific foster parents. We tested whether neural responses in the female auditory forebrain paralleled each of these known behavioral patterns in song-class discrimination. We analyzed spike rates, above background levels, recorded from single units in the L2a subregion of the field L complex of female zebra finches. In subjects raised by genetic parents, spike rates were similar to songs of fathers and unfamiliar male zebra finches, and higher to unfamiliar conspecific over unfamiliar heterospecific songs. In females raised in isolation from male songs, we also found higher spike rates to unfamiliar conspecific over heterospecific songs. In females raised by heterospecific foster parents, spike rates were similar in response to songs of the foster father and unfamiliar males of the foster species, similar between unfamiliar songs of conspecifics and the heterospecific foster species, and higher to unfamiliar songs of the foster species over a third finch species. Thus, in parallel to the experience-dependence of females’ behaviors in response to different male song classes, differences in social experiences can also alter neural response patterns to male song classes in the auditory forebrain of female zebra finches.

► Female zebra finches are selective to species-specific male songs in the L2a forebrain region.
► Females raised without males also show higher spike rates to conspecific over heterospecific songs.
► Females raised by another species show reduced selectivity between songs.
► Songbirds’ experiences alter both behavioral and neural song selectivity.