There is a rich history of behavioral and neurobiological research focused on the ‘syntax’ of birdsong as a model for human language and complex auditory perception. Zebra finches are one of the most widely studied songbird species in this area of investigation. As they produce song syllables in a fixed sequence, it is reasonable to assume that adult zebra finches are also sensitive to the order of syllables within their song; however, results from electrophysiological and behavioral studies provide somewhat mixed evidence on exactly how sensitive zebra finches are to syllable order as compared, say, to syllable structure. Here, we investigate how well adult zebra finches can discriminate changes in syllable order relative to changes in syllable structure in their natural song motifs. In addition, we identify a possible role for experience in enhancing sensitivity to syllable order. We found that both male and female adult zebra finches are surprisingly poor at discriminating changes to the order of syllables within their species-specific song motifs, but are extraordinarily good at discriminating changes to syllable structure (i.e., reversals) in specific syllables. Direct experience or familiarity with a song, either using the bird’s own song (BOS) or the song of a flock mate as the test stimulus, improved both male and female zebra finches’ sensitivity to syllable order. However, even with experience, birds remained much more sensitive to structural changes in syllables. These results help to clarify some of the ambiguities from the literature on the discriminability of changes in syllable order in zebra finches, provide potential insight on the ethological significance of zebra finch song features, and suggest new avenues of investigation in using zebra finches as animal models for sequential sound processing.
Auditory perception Hearing Song motif Syllable sequence Syllable structure
This is a preview of subscription content, log in to check access.
We thank Jane Brown for help with data analysis and figure preparation, Edward Smith for technical expertise, and Bill Idsardi, Juan Uriagereka, and David Vicario for comments on an earlier draft of this manuscript.
This work was funded by a T32 training grant to N.H.P and A.F. (NIDCD T-32 DC00046), and a National Science Foundation award (under Grant No. 1449815) to A.F.
Compliance with ethical standards
This work was conducted in accordance with Association for the Study of Animal Behaviour (ASAB) guidelines and was approved by the Institutional Animal Care and Use Committee (IACUC) (R-15-09), University of Maryland, College Park.
Catchpole CK, Slater PJB (2008) Bird song: biological themes and variations. Cambridge University Press, Second EditionCrossRefGoogle Scholar
Chen J, van Rossum D, ten Cate C (2015) Artificial grammar learning in zebra finches and human adults: XYX versus XXY. Anim Cogn 18:151–164CrossRefPubMedGoogle Scholar
Chen Y, Matheson LE, Sakata JT (2016) Mechanisms underlying the social enhancement of vocal learning in songbirds. Proc Natl Acad Sci 113:6641–6646Google Scholar
Coleman MJ, Mooney R (2004) Synaptic transformations underlying highly selective auditory representations of learned birdsong. J Neurosci 24:7251–7265CrossRefPubMedGoogle Scholar
Danish HH, Aronov D, Fee MS (2017) Rhythmic syllable-related activity in a songbird motor thalamic nucleus necessary for learned vocalizations. PLoS One 12:e0169568CrossRefPubMedPubMedCentralGoogle Scholar
Dooling RJ, Okanoya K (1995) The method of constant stimuli in testing auditory sensitivity in small birds. In: Klump GM, Dooling RJ, Fay RR, Stebbins WC (eds) Methods in comparative psychoacoustics. Birkha¨user–Verlag, Basel, pp 161–169CrossRefGoogle Scholar
Fee MS, Scharff C (2010) The songbird as a model for the generation and learning of complex sequential behaviors. ILAR J 51:362–377CrossRefPubMedGoogle Scholar
Goldstein MH, King AP, West MJ (2003) Social interaction shapes babbling: testing parallels between birdsong and speech. Proc Natl Acad Sci 100:8030–8035CrossRefGoogle Scholar
Gourevitch V, Galanter EA (1967) A significance test for one parameter isosensitivity functions. Psychometrika 32:25–33CrossRefPubMedGoogle Scholar
Griffith SC, Buchanan KL (2010) The zebra finch: the ultimate Australian supermodel. Emu 110:5–12Google Scholar
Hauber ME, Woolley SM, Cassey P, Theunissen FE (2013) Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds. Behav Brain Res 243:184–190CrossRefPubMedPubMedCentralGoogle Scholar
Holveck MJ, Riebel K (2014) Female zebra finches learn to prefer more than one song and from more than one tutor. Anim Behav 88:125–135CrossRefGoogle Scholar
Ikeda MZ, Jeon SD, Cowell RA, Remage-Healey L (2015) Norepinephrine modulates coding of complex vocalizations in the songbird auditory cortex independent of local neuroestrogen synthesis. J Neurosci 35:9356–9368CrossRefPubMedPubMedCentralGoogle Scholar
Immelmann K (1969) Song development in the zebra finch and other estrildid finches In: Hinde RA (ed) Bird vocalizations, Cambridge University Press pp 61–74Google Scholar
Janata P, Margoliash D (1999) Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J Neurosci 19:5108–5118CrossRefPubMedGoogle Scholar
Kazanina N, Phillips C, Idsardi W (2006) The influence of meaning on the perception of speech sounds. Proc Natl Acad Sci 103:11381–11386CrossRefGoogle Scholar
Kriengwatana B, Spierings MJ, ten Cate C (2016) Auditory discrimination learning in zebra finches: effects of sex, early life conditions and stimulus characteristics. Anim Behav 116:99–112CrossRefGoogle Scholar
Lewicki MS (1996) Intracellular characterization of song-specific neurons in the zebra finch auditory forebrain. J Neurosci 16:5854–5863CrossRefGoogle Scholar
Lipkind D, Zai AT, Hanuschkin A, Marcus GF, Tchernichovski O, Hahnloser RHR (2017) Songbirds work around computational complexity by learning song vocabulary independently of sequence. Nat Commun 8:1247CrossRefPubMedPubMedCentralGoogle Scholar
Lohr B, Dooling RJ, Bartone S (2006) The discrimination of temporal fine structure in call-like harmonic sounds by birds. J Comp Psychol 120:239–251CrossRefPubMedGoogle Scholar
Miyawaki K, Strange W, Verbrugge R, Liberman AM, Jenkins JJ, Fujimora O (1975) An effect of linguistic experience: the discrimination of [r] and [l] by native speakers of Japanese and English. Percept Pychophys 18:331–340CrossRefGoogle Scholar
Moore BC (2014) Auditory processing of temporal fine structure: Effects of age and hearing loss. World Scientific, SingaporeCrossRefGoogle Scholar
Mouterde SC, Elie JE, Mathevon N, Theunissen FE (2017) Single neurons in the avian auditory cortex encode individual identity and propagation distance in naturally degraded communication calls. J Neurosci 37:3491–3510CrossRefPubMedPubMedCentralGoogle Scholar
Okanoya K, Tsumaki S, Honda E (2000) Perception of temporal properties in self-generated songs by Bengalese finches (Lonchura striata var domestica). J Comp Psychol 114:239CrossRefPubMedGoogle Scholar
Peh WY, Roberts TF, Mooney R (2015) Imaging auditory representations of song and syllables in populations of sensorimotor neurons essential to vocal communication. J Neurosci 35:5589–5605CrossRefPubMedPubMedCentralGoogle Scholar
Pfenning AR, Hara E, Whitney O, Rivas MV, Wang R, Roulhac PL (2014) Convergent transcriptional specializations in the brain of humans and song-learning birds. Science 346:1256846CrossRefPubMedPubMedCentralGoogle Scholar
van Heijningen CAA, de Visser J, Zuidema W, ten Cate C (2009) Simple rules can explain discrimination of putative recursive syntactic structures by a songbird species. Proc Natl Acad Sci 106:20538–20543Google Scholar
van Heijningen CAA, Chen J, van Laatum I, van der Hulst B, ten Cate C (2013) Rule learning by zebra finches in an artificial grammar learning task: which rule? Anim Cognit 16:165–175CrossRefGoogle Scholar