Song preferences predict the quality of vocal learning in zebra finches

Abstract

In songbirds, learning to sing is a highly social process that likely involves social reward. Here, we hypothesized that the degree to which a juvenile songbird learns a song depends on the degree to which it finds that song rewarding to hear during vocal development. We tested this hypothesis by measuring song preferences in young birds during song learning and then analyzing their adult songs. Song preferences were measured in an operant key-pressing assay. Juvenile male zebra finches (Taeniopygia guttata) had access to two keys, each of which was associated with a higher likelihood of playing the song of their father or that of another familiar adult ("neighbor"). To minimize the effects of exposure on learning, we implemented a reinforcement schedule that allowed us to detect preferences while balancing exposure to each song. On average, the juveniles significantly preferred the father's song early during song learning, before they were themselves singing. At around post-hatch day 60, their preference shifted to the neighbor's song. At the end of the song learning period, we recorded the juveniles' songs and compared them to the father's and the neighbor's song. All of the birds copied father's song. The accuracy with which the father's song was imitated was positively correlated with the peak strength of the preference for the father's song during the sensitive period. Our results show that preference for a social stimulus, in this case a vocalization, predicted social learning during development.

Song Preference in Female and Juvenile Songbirds: Proximate and Ultimate Questions

“…When investigating the correlation between behaviorally expressed preference and the results of song learning, do differences in the choice of behaviors lead to different results? To date, some studies utilized operant conditioning to quantify the tutor song preference ( Terpstra et al, 2004 ; Pilgeram et al, 2021 ; Rodríguez-saltos et al, 2021 ), while others measured birds’ activities including approaching behavior as an indicator of stimulus engagement or attentional state ( Chen et al, 2016 ; Liu et al, 2021 ). Currently, we do not know whether these behaviors capture the same aspect of song preference or whether they share the neural basis.…”

“…It is known from classical studies that male juveniles have a disposition to selectively learn conspecific songs. More recent behavioral and neurobiological studies suggest the relevance of juveniles’ perceptual preference among conspecific songs ( Fujii et al, 2021 ; Liu et al, 2021 ; Pilgeram et al, 2021 ; Rodríguez-saltos et al, 2021 ) as well as the importance of juveniles’ physiological or arousal state during the exposure to the song they are about to learn ( Chen et al, 2016 ; Yanagihara and Yazaki-Sugiyama, 2019 ; Chen and Sakata, 2021 ; Liu et al, 2021 ). These researchers focus on NCM, while also indicating the involvement of the midbrain catecholaminergic system in the processes of memory formation or increased attention to the tutor song.…”

“…Similarly, song-naive zebra finches juveniles prefer their own species song compared to starling songs, when measured by operant behavior associated with song playbacks ( Braaten and Reynolds, 1999 ). In zebra finches, preference for a tutor song (typically father’s song) is also demonstrated with phonotaxis and vocal response assay ( Clayton, 1988 ) as well as key pecking operant conditioning ( Rodríguez-saltos et al, 2021 ). Selective approaches and vocal responses to father’s song was also reported in juvenile Bengalese finches ( Fujii et al, 2021 ).…”

“…Yet, a breakthrough may be provided by cutting-edge studies. By using a combination of carefully controlled live tutoring and well-designed operant conditioning preference tests, it was recently reported that song preference of juveniles in song development predicts the quality of future song imitation ( Rodríguez-saltos et al, 2021 ). Another study from the same group using the same experimental system attempts to reveal the neural mechanisms underlying the tutor song preference and vocal learning ( Pilgeram et al, 2021 ).…”