Manipulations of sensory experiences during development reveal mechanisms underlying vocal learning biases in zebra finches

Abstract

Biological predispositions in learning can bias and constrain the cultural evolution of social and 33 communicative behaviors (e.g., speech and birdsong), and lead to the emergence of behavioral and 34 cultural "universals". For example, surveys of laboratory and wild populations of zebra finches 35 (Taeniopygia guttata) document consistent patterning of vocal elements ("syllables") with respect to 36 their acoustic properties (e.g., duration, mean frequency). Furthermore, such universal patterns are 37 also produced by birds that are experimentally tutored with songs containing randomly sequenced 38 syllables ("tutored birds"). Despite extensive demonstrations of learning biases, much remains to be 39 uncovered about the nature of biological predispositions that bias song learning and production in 40 songbirds. Here we examined the degree to which "innate" auditory templates and/or biases in vocal 41 motor production contribute to vocal learning biases and production in zebra finches. Such 42 contributions can be revealed by examining acoustic patterns in the songs of birds raised without 43 sensory exposure to song ("untutored birds") or of birds that are unable to hear from early in 44 development ("early-deafened birds"). We observed that untutored zebra finches and early-deafened 45 zebra finches produce songs with positional variation in some acoustic features (e.g., mean frequency) 46 that resemble universal patterns observed in tutored birds. Similar to tutored birds, early-deafened 47 birds also produced song motifs with alternation in acoustic features across adjacent syllables. That 48 universal acoustic patterns are observed in the songs of both untutored and early-deafened birds 49 highlights the contribution motor production biases to the emergence of universals in culturally 50 transmitted behaviors.

Phylogeny and mechanisms of shared hierarchical patterns in birdsong

“…Because these birds lacked auditory experiences with an adult conspecific and with their own vocalizations (auditory feedback; both experiences that shape the trajectory of vocal development in songbirds), the song patterns produced by early-deafened birds are independent from learning and reflect biases in vocal motor production. [34][35][36] Consistent with previous studies, syllables produced by earlydeafened canaries were acoustically distinct from those produced by typically reared canaries 33,37,38 (Figure 6A). For example, early-deafened canaries produced syllables that were higher in spectral entropy (F 1,15.8 = 12.5, p = 0.0028) and spectrotemporal entropy (F 1,14.7 = 13.2, p = 0.0026) and marginally higher in mean frequency (F 1,14.5 = 3.1, p = 0.0992) than those produced by typically reared canaries (i.e., canaries from the same laboratory that were tutored and could hear themselves throughout development; Figure 6B).…”

“…We identified motifs in the songs of all zebra finches using previously documented methods. 36,61 Briefly, 2-3 researchers with extensive experience with zebra finch song (L.S.J, J.T.S., and A. Wang) independently identified motifs for all birds and subsequently discussed and agreed upon all motifs used in the study. Zebra finches without consistently identifiable motifs were not included in the analysis.…”

“…To compare acoustic properties of early-deafened and typically-reared birds, we measured five features across all syllable types: duration, mean frequency, spectral entropy, amplitude entropy and spectrotemporal entropy. 36,87,88 Syllable duration is defined as the interval from syllable onset to offset. Mean frequency is the power-weighted average frequency calculated over the spectrum of the entire syllable and is defined as:…”

“…Effect of position on syllable and phrase durations A number of studies of human speech and music and of animal communication have found that the duration of an acoustic element can vary depending on the relative position of the element in the phrase. 4,24,27,36,61,93 Therefore, we conducted analyses that included the ''relative position'' of syllables within phrases.…”

Introductory gestures before songbird vocal displays are shaped by learning and biological predispositions

“…This would predict a correlation across birds between variation in IN number and/or structure and variation in the song that follows. Finally, variation in IN number and structure across birds could also be a result of biological predispositions similar to those involved in the production of elements of song [34,35].…”