Stepwise acquisition of vocal combinatorial capacity in songbirds and human infants

Abstract

Human language, as well as birdsong, relies on the ability to arrange vocal elements in new sequences. However, little is known about the ontogenetic origin of this capacity. Here we track the development of vocal combinatorial capacity in three species of vocal learners, combining an experimental approach in zebra finches (Taeniopygia guttata) with an analysis of natural development of vocal transitions in Bengalese finches (Lonchura striata domestica) and pre-lingual human infants. We find a common, stepwise pattern of acquiring vocal transitions across species. In our first study, juvenile zebra finches were trained to perform one song and then the training target was altered, prompting the birds to swap syllable order, or insert a new syllable into a string. All birds solved these permutation tasks in a series of steps, gradually approximating the target sequence by acquiring new pairwise syllable transitions, sometimes too slowly to accomplish the task fully. Similarly, in the more complex songs of Bengalese finches, branching points and bidirectional transitions in song syntax were acquired in a stepwise fashion, starting from a more restrictive set of vocal transitions. The babbling of pre-lingual human infants showed a similar pattern: instead of a single developmental shift from reduplicated to variegated babbling (that is, from repetitive to diverse sequences), we observed multiple shifts, where each new syllable type slowly acquired a diversity of pairwise transitions, asynchronously over development. Collectively, these results point to a common generative process that is conserved across species, suggesting that the long-noted gap between perceptual versus motor combinatorial capabilities in human infants may arise partly from the challenges in constructing new pairwise vocal transitions.

Figure 1. Syllable rearrangement task

a, Top, sequential training with two songs; bottom, training models. b, Song examples (top) and scatter plots of syllable features (bottom) after source and after learning in one bird. Clusters represent syllable types and lines represent transitions (colors represent transition end syllable). c–d, Daily frequencies (in one bird) of c, source and target songs; d, target bigrams; e, Learning phases in successful birds (means ± s.e.m.; n=8). f, Songs and syntax diagrams during learning (same bird). g, duration of adjustment and extinction according to bigram appearance order. h–j, Same as c, d and f in an unsuccessful bird.

Figure 2. Syllable insertion task

a–b,: Training regime and models. c, Learning outcome in one bird. d–f, Daily frequencies of syllable sequences in one bird: d, Source and target songs; e, target bigrams; f, occurrences of syllable B at bouts’ end (green), start (orange) and middle (red). g, Song examples during learning (same bird). h–j, Means ± s. e. m. (n=10) of h, appearance lags of target bigrams; i, adjustment durations; j, lags between target bigrams’ appearance, adjustment of the 2^nd target bigram, and extinction duration of the source bigram (AA).

Figure 3. Combinatorial learning in Bengalese finches

a–b, Development of bidirectional transitions in two birds. Insets show endpoint syntax. c, Mean ± s.e.m. of appearance lag & adjustment duration in bidirectional transitions (n=7 transitions). d, Frequencies of unidirectional (top, n=16) and bidirectional (bottom, n=7) transitions in early development and at endpoint. e, Top, binary transition matrix (one bird), showing transitions present only early (green), only at endpoint (red), and in both (gray). Bottom, means ± s.e.m. across birds (n=8) of the number of transitions present only early or only at endpoint; f, Developmental changes in the mean number of transitions per syllable (in cases of variable transitions).

Figure 4. Incorporation of new syllables into infants’ babbling utterances

a–b, Frequency of syllable occurrence in reduplicated transitions. a, Data aligned by developmental stage (time zero is the first session with >50% of speech utterances); b, Data aligned by each syllable type’s first appearance. c, Frequency of syllable occurrence at utterance edges. d, New transition types added per syllable type. a–d, Means ± s. e. m. across children (n=9) are deviations from chance level (zero, red dashed line, assessed by bootstrap analysis). Grey lines, fitted linear model.