Bird Vocal Cultures

  • Taxa: birds
  • Species: zebra finches
  • Topics: communication, nonhuman cultures

Culture is typically contrasted from the biological as being conventional—seemingly arbitrary arrangements (linguistic, behavioral, political) versus “hard-wired” instincts (drives, rewards, etc.). This formulation easily equated culture with human behavior, over against animals who are entirely shaped by instinct. But it is now being reformulated, initially through research on our primate cousins, then the locally-learned dialects of cetaceans, and now in the vocal performances of some bird species. Two recent articles in Science advance this perspective on nonhuman culture in concert. A study by Makoto Araki et al takes us into the early auditory experience of juvenile birds as they learn to generate individual songs, distinct from conspecifics but without diverging beyond their own species’ song identity. As with anything cultural, this requires a great deal of locally-based learning, as young birds are tutored in singing by adults. It also involves practices, as juveniles develop “song motifs” that permit detecting conspecific vocalization while also recognizing individual differences. In a move that is oft-gestured at in introductory cultural anthropology courses (certainly my own), the researchers demonstrate the power of culture by asking what happens if those juveniles are raised in a different setting. In this case, they perform a cross-fostering experiment by having Bengalese finches serve as parents for young zebra finches.

Results

“Our findings show that in response to prosodic melodies of adult zebra finch tutors, a subset of neurons in the juvenile zebra finch primary auditory forebrain innately encode silent temporal gap patterns, while a different subset of neurons encode the morphology of song elements. Temporal gap patterns indexed the species specificity of songs and could not be altered by early auditory experience. In contrast, the learning of morphology or acoustic structure of syllables was experience-dependent.” Young zebra finches learn to sing in an adaptive manner, taking on the acoustic conventions of their foster parents, yet do so with a bit of an accent in the timing of gaps between morphological units in the local language. This is fascinating for at least two reasons: (1) this finding speaks to the power of culture to operate on the plasticity of species, molding a biological template into locally distinctive forms; (2) we can see birdsong, which combines various levels of information about identity (species, social group, and individual), as featuring some conventional features. Importantly, too, we can glimpse the type of performative dimensions amongst birds that we already recognize in human cultures. These identities entail varying degrees of fixity, but are often fluidly negotiated and rearticulated over the course of a lifetime as individuals navigate the expectations and opportunities of social life.

This performative dimension is highlighted in the study by Vikram Gadagkar et al, which opens with the image of someone practicing the piano, trying to distinguish right from wrong notes when nothing intrinsically characterizes any one as inherently either good or bad. Birds face this conundrum as they learn to sing and hear the songs of others. Gadagkar et al explored this by monitoring dopamine neurons in singing zebra finches while they manipulated their perception of song quality by inducing distorted auditory feedback information. They tricked the birds into believing they produced distorted syllables. This experiment reveals an internal evaluative system by which birds assess their own vocal performances, suggesting a mechanisms by which juveniles learn to imitate their mentors while also underscoring the conventional aspects of these song cultures. Their results point to a nuanced interpretive process involving “evaluation of auditory feedback against internal performance benchmarks that require, at each step of the song sequence, information about the desired outcome, the actual outcome, and also predicted probability of achieving the desired outcome.” In a social setting structured as a complex acoustical environment—songs locate predators, like barn owls, and report on shifting in-group alliances—the cultural pliancy of this sensory medium allows for the emergence of distinctively performative, interpretive subjects.

Taken together, these studies suggest that a cultural analysis of zebra finches, in the fields rather than the labs, would certainly be warranted and likely quite generative. But more broadly, these works speak to dynamics of animal communication more broadly, especially regarding the matter of how species might establish and reproduce stable cultures. But work in this direction would exactly need to be developed in field settings where social interactions can be mapped and then correlated with the monitoring of individual performance dynamics in lab settings.

On the manifold forms of bird sociality, see Jennifer Ackerman’s The Genius of Birds (2016). Ackerman surveys a massive range of species and highlights the complex work of alliance building and contestation in their diverse social worlds.

Abstracts

Makoto Araki, M. M. Bandi, Yoko Yazaki-Sugiyama, “Mind the Gap: Neural Coding of Species Identity in Birdsong Prosody,” Science 354, no. 6317 (December 2016): 1282–87, https://doi.org/10.1126/science.aah6799.

Juvenile songbirds learn vocal communication from adult tutors of the same species but not from adults of other species. How species-specific learning emerges from the basic features of song prosody remains unknown. In the zebra finch auditory cortex, we discovered a class of neurons that register the silent temporal gaps between song syllables and are distinct from neurons encoding syllable morphology. Behavioral learning and neuronal coding of temporal gap structure resisted song tutoring from other species: Zebra finches fostered by Bengalese finch parents learned Bengalese finch song morphology transposed onto zebra finch temporal gaps. During the vocal learning period, temporal gap neurons fired selectively to zebra finch song. The innate temporal coding of intersyllable silent gaps suggests a neuronal barcode for conspecific vocal learning and social communication in acoustically diverse environments.

Vikram Gadagkar, Pavel A. Puzerey, Ruidong Chen, Eliza Baird-Daniel, Alexander R. Farhang, Jesse H. Goldberg, “Dopamine Neurons Encode Performance Error in Singing Birds,” Science 354, no. 6317 (December 2016): 1278–82, https://doi.org/10.1126/science.aah6837.

Many behaviors are learned through trial and error by matching performance to internal goals. Yet neural mechanisms of performance evaluation remain poorly understood. We recorded basal ganglia—projecting dopamine neurons in singing zebra finches as we controlled perceived song quality with distorted auditory feedback. Dopamine activity was phasically suppressed after distorted syllables, consistent with a worse-than-predicted outcome, and was phasically activated at the precise moment of the song when a predicted distortion did not occur, consistent with a better-than-predicted outcome. Error response magnitude depended on distortion probability. Thus, dopaminergic error signals can evaluate behaviors that are not learned for reward and are instead learned by matching performance outcomes to internal goals.