Abstract
Oscines learn to produce a complex vocalization, the song, which they copy from a conspecific as young birds. The song is an attractive and conspicuous acoustic signal with striking spectral and temporal complexity. The oscine song copying behavior is also remarkable because vocal imitation is a relatively rare ability in vertebrates and because none of the nonavian species can outperform the best oscine mimics. Studies of the neurobiology of song learning have unraveled many of the mechanisms involved in this impressive vocal behavior. Song, however, is only one of the many vocalizations that are produced by oscines. The vocal repertoire of oscines is impressive not only because of the number of vocalizations produced but also because of the flexible production and usage of these sounds. This chapter reviews the vocal behavior of oscines in the framework of animal communication and examines the mechanisms underlying the production and perception of all vocalization types. The chapter also reviews how the auditory system and vocal and social brain networks might be connected to generate appropriate responses to communication calls and song. As a whole, this chapter argues that studies of the mechanisms underlying song learning and also the mechanisms underlying call plasticity, production, and perception are critical for understanding the neuroethology of vocal communication in oscines. Embracing the complexity of the vocal communication system of oscines will enhance our understanding of the brain areas that, until now, have mostly been studied in the context of song imitation.
“Bird calls are the neglected orphans of avian behavioral neurobiology.”– Marler 2004.
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Akutagawa E, Konishi M (2010) New brain pathways found in the vocal control system of a songbird. J Comp Neurol 518(15):3086–3100
Alward BA, Balthazart J, Ball GF (2013) Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc Natl Acad Sci US A 110(48):19573–19578
Amin N, Gill P, Theunissen FE (2010) Role of the zebra finch auditory thalamus in generating complex representations for natural sounds. J Neurophysiol 104(2):784–798
Appeltants D, Ball G, Balthazart J (2002) The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 13:649–653
Aronov D, Andalman AS, Fee MS (2008) A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320(5876):630–634
Ashmore RC, Renk JA, Schmidt MF (2008) Bottom-up activation of the vocal motor forebrain by the respiratory brainstem. J Neurosci 28(10):2613–2623
Baker MC, Bjerke TK, Lampe HU et al (1987) Sexual-response of female yellowhammers to differences in regional song dialects and repertoire sizes. Anim Behav 35:395–401
Bauer EE, Coleman MJ, Roberts TF et al (2008) A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28(6):1509–1522
Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20(3):143–149
Belyk M, Brown S (2017) The origins of the vocal brain in humans. Neuroscience and Biobehav Rev 77:177–193
Benichov JI, Benezra SE, Vallentin D et al (2016) The forebrain song system mediates predictive call timing in female and male zebra finches. Curr Biol 26(3):309–318
Bottjer SW, Miesner EA, Arnold AP (1984) Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224(4651):901–903
Brenowitz EA, Beecher MD (2005) Song learning in birds: diversity and plasticity opportunities and challenges. Trends Neurosci 28(3):127–132
Coleman MJ, Vu ET (2005) Recovery of impaired songs following unilateral but not bilateral lesions of nucleus uvaeformis of adult zebra finches. J Neurobiol 63(1):70–89
Coleman MJ, Roy A, Wild JM et al (2007) Thalamic gating of auditory responses in telencephalic song control nuclei. J Neurosci 27(37):10024–10036
D’Amelio PB, Klumb M, Adreani MN et al (2017) Individual recognition of opposite sex vocalizations in the zebra finch. Sci Rep 7:5579
Daley M, Goller F (2004) Tracheal length changes during zebra finch song and their possible role in upper vocal tract filtering. J Neurobiol 59(3):319–330
Dalziell AH, Magrath RD (2012) Fooling the experts: accurate vocal mimicry in the song of the superb lyrebird Menura novaehollandiae. Anim Behav 83(6):1401–1410
Dunning JL, Maze SE, Atwood EJ et al (2018) Caudal mesopallial neurons in female songbirds bridge sensory and motor brain regions. J Comp Neurol 526(10):1703–1711
Durand SE, Tepper JM, Cheng MF (1992) The shell region of the nucleus ovoidalis: a subdivision of the avian auditory thalamus. J Comp Neurol 323(4):495–518
Düring DN, Elemans CPH (2016) Embodied motor control of avian vocal production In: Suthers R Fitch W Fay R Popper A (eds) Vertebrate Sound Production and Acoustic Communication Springer Handbook of Auditory Research vol 53
Elie JE, Theunissen FE (2015) Meaning in the avian auditory cortex: neural representation of communication calls. Eur J Neurosci 41(5):546–567
Elie JE, Theunissen FE (2016) The vocal repertoire of the domesticated zebra finch: a data-driven approach to decipher the information-bearing acoustic features of communication signals. Anim Cogn 19(2):285–315
Elie JE, Theunissen FE (2018) Zebra finches identify individuals using vocal signatures unique to each call type. Nat Commun 9(1):4026
Elie JE, Soula HA, Mathevon N et al (2011) Dynamics of communal vocalizations in a social songbird the zebra finch (Taeniopygia guttata). J Acoust Sco Am 129(6):4037–4046
Engesser S, Crane JM, Savage JL et al (2015) Experimental evidence for phonemic contrasts in a nonhuman vocal system. PLoS Biol 13(6):e1002171
Engesser S, Ridley AR, Townsend SW (2016) Meaningful call combinations and compositional processing in the southern pied babbler. Proc Natl Acad Sci U S A 113(21):5976–5981
Fitch WT, Huber L, Bugnyar T (2010) Social cognition and the evolution of language: constructing cognitive phylogenies. Neuron 65(6):795–814
Flower TP, Gribble M, Ridley AR (2014) Deception by flexible alarm mimicry in an african bird. Science 344(6183):513–516
Freeberg TM (2008) Complexity in the chick-a-Dee call of carolina chikcadees. Auk 125(4):896–907
Fukushima Y, Aoki K (2000) The role of the dorsomedial nucleus (DM) of intercollicular complex with regard to sexual difference of distance calls in Bengalese finches. Zool Sci 17(9):1231–1238
Gammon DE, Altizer CE (2011) Northern mockingbirds produce syntactical patterns of vocal mimicry that reflect taxonomy of imitated species. J Field Ornithol 82(2):158–164
Gentner TQ (2004) Neural systems for individual song recognition in adult birds. Ann N Y Acad Sci 1016:282–302
Gentner TQ, Hulse SH (1998) Perceptual mechanisms for individual vocal recognition in European starlings Sturnus vulgaris. Anim Behav 56(3):579–594
Gentner TQ, Margoliash D (2003) Neuronal populations and single cells representing learned auditory objects. Nature 424(6949):669–674
Gill SA, Bierema AM, Hauber M (2013) On the meaning of alarm calls: a review of functional reference in avian alarm calling. Ethology 119(6):449–461
Gobes SM, Bolhuis JJ (2007) Birdsong memory: a neural dissociation between song recognition and production. Curr Biol 17(9):789–793
Gobes SM, Zandbergen MA, Bolhuis JJ (2010) Memory in the making: localized brain activation related to song learning in young songbirds. Proc Roy Soc B-Biol Sci 277(1698):3343–3351
Goller M, Shizuka D (2018) Evolutionary origins of vocal mimicry in songbirds. Evol Lett 2(4):417–426
Goller F, Mallinckrodt MJ, Torti SD (2004) Beak gape dynamics during song in the zebra finch. J Neurobiol 59(3):289–303
Goodson JL (2005) The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 48(1):11–22
Goodson JL, Kelly AM, Kingsbury MA et al (2012) An aggression-specific cell type in the anterior hypothalamus of finches. Proc Natl Acad Sci 109(34):13847–13852
Griesser M, Wheatcroft D, Suzuki TN (2018) From bird calls to human language: exploring the evolutionary drivers of compositional syntax. Curr Opin Behav Sci 21:6–12
Hahnloser RH, Kozhevnikov AA, Fee MS (2002) An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419:65–70
Hamaguchi K, Mooney R (2012) Recurrent interactions between the input and output of a songbird cortico-basal ganglia pathway are implicated in vocal sequence variability. J Neurosci 32:11671–11687
Hara E, Kubikova L, Hessler NA et al (2007) Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur J Neurosci 25(11):3406–3416
Hessler NA, Doupe AJ (1999) Social context modulates singing-related neural activity in the songbird forebrain. Nat Neurosci 2(3):209–211
Hisey E, Kearney MG, Mooney R (2018) A common neural circuit mechanism for internally guided and externally reinforced forms of motor learning. Nat Neurosci 21(4):589–597
Hoffmann LA, Saravanan V, Wood AN et al (2016) Dopaminergic contributions to vocal learning. J Neurosci 36(7):2176–2189
Honarmand M, Riebel K, Naguib M (2015) Nutrition and peer group composition in early adolescence: impacts on male song and female preference in zebra finches. Anim Behav 107:147–158
Hsu A, Woolley SM, Fremouw TE et al (2004) Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons. J Neurosci 24(41):9201–9211
Janik VM (2014) Cetacean vocal learning and communication. Curr Opin Neurobiol 28:60–65
Janik VM, Slater PJB (1997) Vocal learning in mammals. Adv Stud Behav 26:59–99
Jarvis ED (2013) Evolution of brain pathways for vocal learning in birds and humans. In: Bolhuis J, Everaert M (eds) Birdsong speech and language: exploring the evolution of mind and brain. MIT Press, Boston, pp 63–107
Jarvis ED, Yu J, Rivas MV et al (2013) Global view of the functional molecular organization of the avian cerebrum: mirror images and functional columns. J Comp Neurol 521(16):3614–3665
Jeanne JM, Thompson JV, Sharpee TO, et al (2011) Emergence of learned categorical representations within an auditory forebrain circuit. J Neurosci 31(7):2595–2606
Kingsbury MA, Kelly AM, Schrock SE et al (2011) Mammal-like organization of the avian midbrain central gray and a reappraisal of the intercollicular nucleus. PLoS One 6(6):e20720
Knörnschild M, Nagy M, Metz M et al (2010) Complex vocal imitation during ontogeny in a bat. Biol Lett 6(2):156–159
Konishi M (2003) Coding of auditory space. Ann Rev Neurosci 26:31–55
Kroodsma DE, Konishi M (1991) A suboscine bird (eastern phoebe Sayornis phoebe) develops normal song without auditory feedback. Anim Behav 42:477–487
Krützfeldt NO, Logerot P, Kubke MF et al (2010) Connections of the auditory brainstem in a songbird Taeniopygia guttata. II projections of nucleus angularis and nucleus laminaris to the superior olive and lateral lemniscal nuclei. J Comp Neurol 518(11):2135–2148
Langmore NE, Maurer G, Adcock GJ et al (2008) Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62(7):1689–1699
Larsen ON, Goller F (2002) Direct observation of syringeal muscle function in songbirds and a parrot. J Exp Biol 205(1):25–35
Lehongre K, Aubin T, Robin S et al (2008) Individual signature in canary songs: contribution of multiple levels of song structure. Ethology 114(5):425–435
Lewandowski B, Vyssotski A, Hahnloser RH et al (2013) At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing production and learning. Journal of physiology Paris 107(3):178–192
Ligout S, Dentressangle F, Mathevon N et al (2016) Not for parents only: begging calls allow nest-mate discrimination in juvenile zebra finches. Ethology 122:193–206
Long MA, Fee MS (2008) Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456(7219):189–194
Maddox RK, Billimoria CP, Perrone BP et al (2012) Competing sound sources reveal spatial effects in cortical processing. PLoS Biol 10(5):e1001319
Mandelblat-Cerf Y, Las L, Denissenko N et al (2014) A role for descending auditory cortical projections in songbird vocal learning. elife 3:e02152
Marler P (1956) The voice of the chaffinch and its function as a language. Ibis 98:231–261
Marler P (1982) Avian and primate communication: the problem of natural categories. Neurosci Biobehav Rev 6(1):87–94
Marler P (1967) Animal communication signals. Science 157(3790):769–774
Marler P (1970) A comparative approach to vocal learning: song development in white-crowned sparrows. J Comp Physiol Psychol 71(22):1–25
Marler P (1997) Three models of song learning: evidence from behavior. J Neurobiol 33(5):501–516
Marler P (2004) Bird calls: their potential for neurobiology. In: Zeigler HP, Marler P (eds) Behavioral neurobiology of birdsong. The New York Academy of Science, New York, pp 31–44
Meliza CD, Margoliash D (2012) Emergence of selectivity and tolerance in the avian auditory cortex. J Neurosci 32(43):15158–15168
Mello C, Vates G, Okuhata S et al (1998) Descending auditory pathways in the adult male zebra finch. J Comp Neurol 395:137–160
Menardy F, Touiki K, Dutrieux G et al (2012) Social experience affects neuronal responses to male calls in adult female zebra finches. Eur J Neurosci 35(8):1322–1336
Miller DB (1979a) The acoustic basis of mate recognition by female zebra finches (Taeniopygia guttata). Anim Behav 27:376–380
Miller DB (1979b) Long-term recognition of fathers song by female zebra finches. Nature 280(5721):389–391
Moore RC, Lee T, Theunissen FE (2013) Noise-invariant neurons in the avian auditory cortex: hearing the song in noise. Plos Comp Biol 9(3):e1002942
Mouterde SC, Elie JE, Mathevon N et al (2017) Single neurons in the avian auditory cortex encode individual identity and propagation distance in naturally degraded communication calls. J Neurosci 37(13):3491–3510
Nottebohm F, Stokes TM, Leonard CM (1976) Central control of song in canary Serinus canarius. J Comp Neurol 165(4):457–486
Nottebohm F, Kelley D, Paton J (1982) Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol 207:344–357
Perez EC, Elie JE, Boucaud IC et al (2015) Physiological resonance between mates through calls as possible evidence of empathic processes in songbirds. Horm Behav 75:130–141
Phan ML, Pytte CL, Vicario DS (2006) Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc Natl Acad Sci 103(4):1088–1093
Potvin DA, Ratnayake CP, Radford AN et al (2018) Birds learn socially to recognize heterospecific alarm calls by acoustic association. Curr Biol 28(16):2632
Riede T, Goller F (2010) Peripheral mechanisms for vocal production in birds - differences and similarities to human speech and singing. Brain Lang 115(1):69–80
Riede T, Schilling N, Goller F (2013) The acoustic effect of vocal tract adjustments in zebra finches. J Comp Physiol A 199(1):57–69
Riters LV, Alger SJ (2004) Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song. Cell Tissue Res 316(1):35–44
Roberts TF, Hisey E, Tanaka M et al (2017) Identification of a motor-to-auditory pathway important for vocal learning. Nat Neurosci 20(7):978–986
Schmidt MF, Wild JM (2014) The respiratory-vocal system of songbirds. anatomy physiology and neural control Prog Brain Res 212:297–335
Schneider DM, Woolley SM (2013) Sparse and background-invariant coding of vocalizations in auditory scenes. Neuron 79(1):141–152
Searcy WA, Beecher MD (2009) Song as an aggressive signal in songbirds. Anim Behav 78(6):1281–1292
Seyfarth RM, Cheney DL (2010) Production usage and comprehension in animal vocalizations. Brain Lang 115(1):92–100
Sewards TV, Sewards MA (2003) Representations of motivational drives in mesial cortex medial thalamus hypothalamus and midbrain. Brain Res Bull 61(1):25–49
Shaevitz SS, Theunissen FE (2007) Functional connectivity between auditory areas field L and CLM and song system nucleus HVC in anesthetized zebra finches. J Neurophysiol 98(5):2747–2764
Simpson HB, Vicario DS (1990) Brain pathways for learned and unlearned vocalizations differ in zebra finches. J Neurosci 10(5):1541–1556
Sitt JD, Amador A, Goller F et al (2008) Dynamical origin of spectrally rich vocalizations in birdsong. Physic Rev E 78(1):e011905
Slabbekoorn H, Smith TB (2002) Bird song ecology and speciation. Phylos T Roy Soc B 357(1420):493–503
Slater PJ, Jones AE (1995) The timing of song and distance call learning in zebra finches. Anim Behav 49(2):548–550
Sober JS, Wohlgemuth MJ, Brainard MS (2008) Central contributions to acoustic variation in birdsong. J Neurosci 28(41):10370–10379
Stoeger AS, Manger P (2014) Vocal learning in elephants: neural bases and adaptive context. Curr Opin Neurobiol 28:101–107
Suthers RA, Goller F, Hartley RS (1994) Motor dynamics of song production by mimic thrushes. J Neurobiol 25(8):917–936
Suzuki TN (2018) Alarm calls evoke a visual search image of a predator in birds. Proc Natl Acad Sci 115(7):1541–1545
Suzuki TN, Wheatcroft D, Griesser M (2018) Call combinations in birds and the evolution of compositional syntax. PLoS Biol 16(8):e2006532
Tanaka M, Sun FM, Li YL et al (2018) A mesocortical dopamine circuit enables the cultural transmission of vocal behavior. Nature 563(7729):117–119
Ter Maat A, Trost L, Sagunsky H et al (2014) Zebra finch mates use their forebrain song system in unlearned call communication. PLoS One 9(10):e109334
Vates GE, Broome BM, Mello CV et al (1996) Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata). J Comp Neurol 366:613–642
Vicario DS, Simpson HB (1995) Electrical stimulation in forebrain nuclei elicits learned vocal patterns in songbirds. J Neurophysiol 73(6):2602–2607
Vicario DS, Naqvi NH, Raksin JN (2001) Behavioral discrimination of sexually dimorphic calls by male zebra finches requires an intact vocal motor pathway. J Neurobiol 47(2):109–120
Vignal C, Mathevon N, Mottin S (2004) Audience drives male songbird response to partner’s voice. Nature 430(6998):448–451
Villain AS, Boucaud IC, Bouchut C et al (2015) Parental influence on begging call structure in zebra finches (Taeniopygia guttata): evidence of early vocal plasticity. Roy Soc Open Sci 2(11):e150497
Vu ET, Mazurek ME, Kuo YC (1994) Identification of a forebrain motor programming network for the learned song of zebra finches. J Neurosci 14(11):6924–6934
Wang L, Narayan R, Grana G et al (2007) Cortical discrimination of complex natural stimuli: can single neurons match behavior? J Neurosci 27(3):582–589
Wang Y, Brzozowska-Prechtl A, Karten HJ (2010) Laminar and columnar auditory cortex in avian brain. Proc Natl Acad Sci 107(28):12676–12681
Wild JM (1994a) The auditory-vocal-respiratory axis in birds. Brain Behav Evol 44(4):192–209
Wild JM (1994b) Visual and somatosensory inputs to the avian song system via nucleus uvaeformis (Uva) and a comparison with the projections of a similar thalamic nucleus in a nonsongbird Columba livia. J Comp Neurol 349(4):512–535
Wild JM (2017) The ventromedial hypothalamic nucleus in the zebra finch (Taeniopygia guttata): afferent and efferent projections in relation to the control of reproductive behavior. J Comp Neurol 525(12):2657–2676
Wild JM, Botelho JF (2015) Involvement of the avian song system in reproductive behavior. Biol Lett 11(12):e20150773
Wild JM, Krützfeldt NE (2010) Neocortical-like organization of avian auditory ‘cortex’. Brain Behav Evol 76(2):89–92
Wild JM, Krützfeldt NE (2012) Trigeminal and telencephalic projections to jaw and other upper vocal tract premotor neurons in songbirds: sensorimotor circuitry for beak movements during singing. J Comp Neurol 520(3):590–605
Wild JM, Li DF, Eagleton C (1997) Projections of the dorsomedial nucleus of the intercollicular complex (DM) in relation to respiratory-vocal nuclei in the brainstem of pigeon (Columba livia) and zebra finch (Taeniopygia guttata). J Comp Neurol 377(3):392–413
Woolley SC, Doupe AJ (2008) Social context - induced song variation affects female behavior and gene expression. PLoS Biol 6(3):525–537
Woolley SM, Portfors CV (2013) Conserved mechanisms of vocalization coding in mammalian and songbird auditory midbrain. Hear Res 305:45–56
Woolley SM, Gill PR, Fremouw T et al (2009) Functional groups in the avian auditory system. J Neurosci 29(9):2780–2793
Woolley SC, Rajan R, Joshua M et al (2014) Emergence of context-dependent variability across a basal ganglia network. Neuron 82(1):208–223
Xiao L, Chattree G, Oscos FG et al (2018) A basal ganglia circuit sufficient to guide birdsong learning. Neuron 98(1):208–221
Yanagihara S, Yazaki-Sugiyama Y (2016) Auditory experience-dependent cortical circuit shaping for memory formation in bird song learning. Nat Commun 7:e11946
Zann R (1985) Ontogeny of the zebra finch distance call. 1 effects of cross-fostering to Bengalese finches. Zeitschrift Fur Tierpsychologie (Journal of Comparative Ethology) 68(1):1–23
Zann R (1990) Song and call learning in wild zebra finches in south-East Australia. Anim Behav 40:811–828
Zann R (1996) The Zebra finch: a synthesis of field and laboratory studies. Oxford University Press, Oxford
Acknowledgements
The authors thank Profs. Martin Wild, Marc Schmidt, Sarah Woolley, and Jon Sakata for their insightful comments and feedback on draft versions of this chapter.
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Julie Elie declares that she has no conflict of interest.
Frédéric Theunissen declares that he has no conflict of interest.
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Elie, J.E., Theunissen, F.E. (2020). The Neuroethology of Vocal Communication in Songbirds: Production and Perception of a Call Repertoire. In: Sakata, J., Woolley, S., Fay, R., Popper, A. (eds) The Neuroethology of Birdsong. Springer Handbook of Auditory Research, vol 71. Springer, Cham. https://doi.org/10.1007/978-3-030-34683-6_7
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