Diurnal oscillation of vocal development associated with clustered singing by juvenile songbirds

Abstract

Spaced practice affects learning efficiency in humans and other animals. However, it is not well understood how spaced practice contributes to learning during development. Here, we show the behavioral significance of singing frequency in song development in a songbird, the zebra finch. Songbirds learn a complex song pattern by trial-and-error vocalizations as self-motivated practice, which is executed over a thousand times per day during the sensitive period of vocal learning. Notably, juveniles generate songs with a high frequency of singing in clusters with dense singing, whereas adults sing with low frequency in short clusters. This juvenile-specific clustered singing was characterized by clear separations of daily time for intense practice and rest. During the epochs of vocal practice in juveniles, the song structure approached that of song produced at the end of the day. In contrast, during the epochs of vocal rest, the structure of juvenile songs regressed toward that of songs produced at the beginning of the day, indicating a dynamic progression and regression of song development over the course of the day. When the singing frequency was manipulated to decrease it at the juvenile stage, the oscillation rate of song development was dramatically reduced. Although the juvenile-specific clustered singing occurred in non-tutored socially isolated birds or those with auditory deprivation, the diurnal oscillation of vocal development was only observed in non-tutored isolated juveniles. These results show the impact of 'self-motivated' vocal practice on diurnal song developmental plasticity, modulated by the amount of vocal output and auditory feedback.

Unstable neurons underlie a stable learned behavior

“…The change in the song motor pattern occurs primarily over intervals of sleep, and we have shown that adult song behavior also undergoes microscopic shifts in sleep. Our results may be related to a previous observation: as juveniles learn to sing, their songs progress through a day of practice 41 , but degrade slightly over intervals of sleep 42 . The depth of this overnight “backsliding” is positively correlated with the eventual success of song learning–indicating that nighttime song rearrangements are important for learning.…”

Vocal practice regulates singing activity–dependent genes underlying age-independent vocal learning in songbirds

“…Singing prevention was highly effective: normal birds produce over 60,000 song bouts during the sensorimotor learning period (approximately 1,000 bouts/day × 60 days) [ 6 ], while the singing prevention birds produced less than 0.1% of this output (24–485 song bouts, mean = 279.0 bouts). When the birds were released from singing prevention at adulthood, they produced “age-unmatched” immature songs with highly variable acoustics and sequence of syllables, i.e., subsong or early plastic-like song ( Fig 1B ).…”

“…In a closed-ended vocal learner songbird, like the zebra finch, the time window of the sensorimotor learning phase lasts 2 months, beginning in juveniles at 30–45 post hatching day (phd) and ending in adulthood at 90–100 phd with the production of crystallized motif song patterns that are then maintained throughout life ( Fig 1A ). During the sensorimotor learning phase, zebra finches produce approximately 1,000 song renditions in a day through self-motivated vocal practice [ 6 – 8 ].…”

Singing activity‐driven Arc expression associated with vocal acoustic plasticity in juvenile songbird

“…To segregate potential effects of the song quality and cumulative singing amount on Arc expression, an experiment examining Arc expression in deafened juveniles during afternoon singing may be crucial. Diurnal syllable acoustic shift is significantly decreased in early‐deafened compared with intact juveniles (Ohgushi et al., ). Therefore, when early‐deafened juveniles freely sing until afternoon period, they accumulate total diurnal singing amount but their song quality is still highly variable due to no auditory feedback.…”

“…Juvenile male zebra finches develop their song from highly variable vocalizations to achieve the stereotyped acoustic structures of adult crystallized song ( Figure 1a) (Immelmann, 1969;Price, 1979). Song acquisition is achieved through thousands of self-motivated singing utterances during the critical period of vocal learning (Johnson, Soderstrom, & Whitney, 2002;Ohgushi, Mori, & Wada, 2015). The acoustic features of song syllables are highly variable during the early plastic song phase (40-60 posthatching days [phd]), compared with those in the crystallized song produced at adulthood (Deregnaucourt et al, 2004;Wood, Osseward, Roseberry, & Perkel, 2013).…”