The origins of vocal learning: New sounds, new circuits, new cells

We do not know how vocal learning came to be, but it is such a salient trait in human evolution that many have tried to imagine it. In primates this is difficult because we are the only species known to possess this skill. Songbirds provide a richer and independent set of data. I use comparative data and ask broad questions: How does vocal learning emerge during ontogeny? In what contexts? What are its benefits? How did it evolve from unlearned vocal signals? How was brain anatomy altered to enable vocal learning? What is the relation of vocal learning to adult neurogenesis? No one has described yet a circuit or set of circuits that can master vocal learning, but this knowledge may soon be within reach. Moreover, as we uncover how birds encode their learned song, we may also come closer to understanding how we encode our thoughts.

[1]  R. Doty,et al.  Lateralization in the nervous system , 1977 .

[2]  F. Nottebohm,et al.  Brain space for a learned task , 1981, Brain Research.

[3]  E. Nordeen,et al.  Projection neurons within a vocal motor pathway are born during song learning in zebra finches , 1988, Nature.

[4]  K. Immelmann Song development in the zebra finch and other estrildid finches , 1969 .

[5]  L. A. Eales Song learning in zebra finches: some effects of song model availability on what is learnt and when , 1985, Animal Behaviour.

[6]  S. Healy,et al.  Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  Louis Lefebvre,et al.  Song complexity correlates with learning ability in zebra finch males , 2008, Animal Behaviour.

[8]  W. Calder,et al.  Respiration during song in the canary (Serinus canaria). , 1970, Comparative biochemistry and physiology.

[9]  F. Goller,et al.  A new mechanism of sound generation in songbirds. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A. Kappers Avian brains and a new understanding of vertebrate brain evolution , 2022 .

[11]  W. H. Thorpe,et al.  THE LEARNING OF SONG PATTERNS BY BIRDS, WITH ESPECIAL REFERENCE TO THE SONG OF THE CHAFFINCH FRINGILLA COELEBS , 2008 .

[12]  A. Zahavi Mate selection-a selection for a handicap. , 1975, Journal of theoretical biology.

[13]  L. A. Eales Do zebra finch males that have been raised by another species still tend to select a conspecific song tutor? , 1987, Animal Behaviour.

[14]  J. Verner Complex song repertoire of male long billed marsh wrens in eastern washington usa , 1975 .

[15]  P. Marler,et al.  Song structure without auditory feedback: emendations of the auditory template hypothesis , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  Laasya Samhita The Handicap Principle , 2010 .

[17]  F. Nottebohm,et al.  Reversal of hypoglossal dominance in canaries following unilateral syringeal denervation , 1979, Journal of comparative physiology.

[18]  P. Marler Birdsong and speech development: could there be parallels? , 1970, American scientist.

[19]  P. Marler,et al.  The Role of Song Phonology and Syntax in Vocal Learning Preferences in the Song Sparrow, Melospiza melodia , 2010 .

[20]  J. Cynx,et al.  Amplitude regulation of vocalizations in noise by a songbird,Taeniopygia guttata , 1998, Animal Behaviour.

[21]  F Goller,et al.  Inspiratory muscle activity during bird song. , 1998, Journal of neurobiology.

[22]  F Goller,et al.  The neuromuscular control of birdsong. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  M. D. Beecher,et al.  Mate, neighbour and stranger songs: a female song sparrow perspective , 1999, Animal Behaviour.

[24]  F. Nottebohm,et al.  Variable Food Begging Calls Are Harbingers of Vocal Learning , 2009, PloS one.

[25]  A. C. Yu,et al.  Temporal Hierarchical Control of Singing in Birds , 1996, Science.

[26]  P. Marler,et al.  Species-universal microstructure in the learned song of the swamp sparrow (Melospiza georgiana) , 1984, Animal Behaviour.

[27]  Felix Naef,et al.  Freedom and Rules: The Acquisition and Reprogramming of a Bird's Learned Song , 2005, Science.

[28]  P. Marler,et al.  Sound transmission and its significance for animal vocalization , 1977, Behavioral Ecology and Sociobiology.

[29]  W. A. Cox,et al.  A Phylogenomic Study of Birds Reveals Their Evolutionary History , 2008, Science.

[30]  L. Baptista,et al.  Social interaction, sensitive phases and the song template hypothesis in the white-crowned sparrow , 1984, Animal Behaviour.

[31]  F. Nottebohm,et al.  Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. , 1986, Behavioral and neural biology.

[32]  D. Kroodsma,et al.  Ecology and evolution of acoustic communication in birds , 1997 .

[33]  D. Vicario Organization of the zebra finch song control system: Functional organization of outputs from nucleus robustus archistriatalis , 1991, The Journal of comparative neurology.

[34]  P. Marler,et al.  Song Development in Hand-Raised Oregon Juncos , 1962 .

[35]  A. Arnold,et al.  Forebrain lesions disrupt development but not maintenance of song in passerine birds. , 1984, Science.

[36]  M. Konishi The role of auditory feedback in the control of vocalization in the white-crowned sparrow. , 1965, Zeitschrift fur Tierpsychologie.

[37]  F. Nottebohm,et al.  Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[38]  William Rowan,et al.  The Study of Instinct , 1953 .

[39]  Donald E. Kroodsma,et al.  Vocal Virtuosity in the Brown Thrasher , 1977 .

[40]  M. Hauser,et al.  The design of animal communication , 1999 .

[41]  Fernando Nottebohm,et al.  Continental Patterns of Song Variability in Zonotrichia capensis: Some Possible Ecological Correlates , 1975, The American Naturalist.

[42]  B. McCowan,et al.  Spontaneous vocal mimicry and production by bottlenose dolphins (Tursiops truncatus): evidence for vocal learning. , 1993, Journal of comparative psychology.

[43]  E Borg,et al.  The middle-ear muscles. , 1989, Scientific American.

[44]  F. Nottebohm,et al.  Left hypoglossal dominance in the control of canary and white-crowned sparrow song , 1976, Journal of comparative physiology.

[45]  L. A. Eales Song learning in female-raised zebra finches: another look at the sensitive phase , 1987, Animal Behaviour.

[46]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[47]  Michael S. Brainard,et al.  Online Contributions of Auditory Feedback to Neural Activity in Avian Song Control Circuitry , 2008, The Journal of Neuroscience.

[48]  M. A. Cunningham,et al.  The Biology of Bird-Song Dialects , 1985, Behavioral and Brain Sciences.

[49]  Dennis Hasselquist,et al.  POLYGYNY IN GREAT REED WARBLERS: A LONG-TERM STUDY OF FACTORS CONTRIBUTING TO MALE FITNESS , 1998 .

[50]  P. Marler,et al.  Culturally Transmitted Patterns of Vocal Behavior in Sparrows , 1964, Science.

[51]  P. Marler Three models of song learning: evidence from behavior. , 1997, Journal of neurobiology.

[52]  Bijan Pesaran,et al.  The role of nonlinear dynamics of the syrinx in the vocalizations of a songbird , 1998, Nature.

[53]  M. Fee,et al.  Using temperature to analyze temporal dynamics in the songbird motor pathway , 2008, Nature.

[54]  Tamás Székely,et al.  Evolutionary changes in a song control area of the brain (HVC) are associated with evolutionary changes in song repertoire among European warblers (Sylviidae) , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[55]  Michale S Fee,et al.  A Specialized Forebrain Circuit for Vocal Babbling in the Juvenile Songbird , 2008, Science.

[56]  G. E. Vates,et al.  Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata) , 1996, The Journal of comparative neurology.

[57]  E. Morton Ecological Sources of Selection on Avian Sounds , 1975, The American Naturalist.

[58]  P. Marler,et al.  Innate differences in singing behaviour of sparrows reared in isolation from adult conspecific song , 1985, Animal Behaviour.

[59]  R. Bertram,et al.  Auditory-Dependent Vocal Recovery in Adult Male Zebra Finches Is Facilitated by Lesion of a Forebrain Pathway That Includes the Basal Ganglia , 2007, The Journal of Neuroscience.

[60]  P. Tyack,et al.  Whistle repertoires of two bottlenosed dolphins, Tursiops truncatus: mimicry of signature whistles? , 1986, Behavioral Ecology and Sociobiology.

[61]  Fernando Nottebohm,et al.  THE SONG OF THE CHINGOLO, ZOiVOTRICHlA CAPENSIS, IN ARGENTINA: DESCRIPTION AND EVALUATION OF A SYSTEM OF DIALECTS , 1969 .

[62]  D. Bambagioni,et al.  Vocalization-related stapedius muscle activity in different age chickens (Gallus gallus), and its role in vocal development , 1990, Brain Research.

[63]  F. N. Robinson,et al.  Vocal mimicry and the evolution of bird song , 1975 .

[64]  R. Payne,et al.  Songs of Humpback Whales , 1971, Science.

[65]  F. Nottebohm,et al.  A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  D. Kroodsma Reproductive Development in a Female Songbird: Differential Stimulation by Quality of Male Song , 1976, Science.

[67]  M. A. Cunningham,et al.  Reproductive behaviour of female white-crowned sparrows: effect of dialects and synthetic hybrid songs , 1987, Animal Behaviour.

[68]  R. Suthers Contributions to birdsong from the left and right sides of the intact syrinx , 1990, Nature.

[69]  M. C. Baker,et al.  Early Experience Determines Song Dialect Responsiveness of Female Sparrows , 1981, Science.

[70]  F. Nottebohm,et al.  Production and survival of projection neurons in a forebrain vocal center of adult male canaries , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  F. Nottebohm,et al.  ALLOZYMIC AND MORPHOLOGICAL VARIATION IN POPULATION SAMPLES OF RUFOUS‐COLLARED SPARROW, ZONOTRICHIA CAPENSIS, IN RELATION TO VOCAL DIALECTS , 1976, Evolution; international journal of organic evolution.

[72]  Masakazu Konishi,et al.  The Role of Auditory Feedback in the Vocal Behavior of the Domestic Fowl1 , 1963, Zeitschrift für Tierpsychologie.

[73]  K. D. Punta,et al.  An ultra-sparse code underlies the generation of neural sequences in a songbird , 2002 .

[74]  P. Marler,et al.  Song learning in canaries. , 1977 .

[75]  F. Nottebohm,et al.  Central control of song in the canary, Serinus canarius , 1976, The Journal of comparative neurology.

[76]  Age- and behavior-related variation in volumes of song control nuclei in male European starlings. , 1996, Journal of neurobiology.

[77]  J. W. Boughman,et al.  Vocal learning by greater spear–nosed bats , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  D. Kroodsma,et al.  The Ecology of Song Improvisation as Illustrated by North American Sedge Wrens , 1999 .

[79]  A. Doupe,et al.  Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations , 2000, Nature.

[80]  P. Marler,et al.  Song "Dialects" in Three Populations of White-Crowned Sparrows , 1962 .

[81]  D Margoliash,et al.  Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[82]  Eric Bonabeau The handicap principle , 1998, Complex..

[83]  Fernando Nottebohm,et al.  Juvenile zebra finches can use multiple strategies to learn the same song , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[84]  S. Elizabeth Campbell,et al.  Territory tenure in song sparrows is related to song sharing with neighbours, but not to repertoire size , 2000, Animal Behaviour.

[85]  E. Nordeen,et al.  Individual variation in neuron number predicts differences in the propensity for avian vocal imitation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[86]  J. F. Prather,et al.  Precise auditory–vocal mirroring in neurons for learned vocal communication , 2008, Nature.

[87]  D. Kroodsma,et al.  Song development by grey catbirds , 1997, Animal Behaviour.

[88]  C. Chapuis L’influence du milieu sur les émissions vocales des oiseaux : L’évolution des chants en forêt équatoriale , 1971, La Terre et La Vie, Revue d'Histoire naturelle.

[89]  Katherine Ralls,et al.  Vocalizations and vocal mimicry in captive harbor seals, Phoca vitulina , 1985 .

[90]  P. Marler A comparative approach to vocal learning: Song development in white-crowned sparrows. , 1970 .

[91]  J. Wingfield,et al.  Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. , 1987, Behavioral and neural biology.

[92]  P. Marler,et al.  Selective Vocal Learning in a Sparrow , 1977, Science.

[93]  T. Nick,et al.  Top-down regulation of plasticity in the birdsong system: "premotor" activity in the nucleus HVC predicts song variability better than it predicts song features. , 2008, Journal of neurophysiology.

[94]  THE NATURE AND CHARACTERISTICS OF SUB-SONG , 2007 .

[95]  J. Ford,et al.  Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska , 2002, Animal Behaviour.

[96]  David C. Airey,et al.  Greater song complexity is associated with augmented song system anatomy in zebra finches , 2000, Neuroreport.

[97]  F. Nottebohm,et al.  Connections of vocal control nuclei in the canary telencephalon , 1982, The Journal of comparative neurology.

[98]  Jeffrey Podos,et al.  Song Learning, Early Nutrition and Sexual Selection in Songbirds , 1998 .

[99]  F. Nottebohm,et al.  Dynamics of the Vocal Imitation Process: How a Zebra Finch Learns Its Song , 2001, Science.

[100]  D. Vicario,et al.  Contributions of syringeal muscles to respiration and vocalization in the zebra finch. , 1991, Journal of neurobiology.

[101]  Louis M. Herman,et al.  Vocal mimicry of computer-generated sounds and vocal labeling of objects by a bottlenosed dolphin, Tursiops truncatus. , 1984, Journal of comparative psychology.

[102]  F. Nottebohm,et al.  Neural lateralization of vocal control in a passerine bird. I. Song. , 1971, The Journal of experimental zoology.

[103]  A white canary on Mount Acropolis , 1996, Journal of Comparative Physiology A.

[104]  P. Marler,et al.  Sparrows Learn Adult Song and More from Memory , 1981, Science.

[105]  F. Nottebohm Neural lateralization of vocal control in a passerine bird , 1971 .

[106]  Fernando Nottebohm,et al.  A learning program that ensures prompt and versatile vocal imitation , 2007, Proceedings of the National Academy of Sciences.

[107]  F. Nottebohm,et al.  Targeted Neuronal Death Affects Neuronal Replacement and Vocal Behavior in Adult Songbirds , 2000, Neuron.

[108]  E. Balaban,et al.  Bird song syntax: learned intraspecific variation is meaningful. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[109]  H. Williams,et al.  Timbre control in zebra finch (Taeniopygia guttata) song syllables. , 1989, Journal of comparative psychology.

[110]  F. Nottebohm,et al.  Population differences in complexity of a learned skill are correlated with the brain space involved. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[111]  P. Marler,et al.  A species-specific acoustic cue for selective song learning in the white-crowned sparrow , 2000, Animal Behaviour.

[112]  P. Marler,et al.  Role of auditory feedback in canary song development. , 1977, Journal of comparative and physiological psychology.

[113]  H. Williams,et al.  Temporal patterning of song production: participation of nucleus uvaeformis of the thalamus. , 1993, Journal of neurobiology.

[114]  Georg B. Keller,et al.  Rapid Interhemispheric Switching during Vocal Production in a Songbird , 2008, PLoS biology.

[115]  J. Poole,et al.  Animal behaviour: Elephants are capable of vocal learning , 2005, Nature.

[116]  J. A. Paton,et al.  Respiratory gating of activity in the avian vocal control system , 1982, Brain Research.

[117]  F. Nottebohm 2 – Asymmetries in Neural Control of Vocalization in the Canary , 1977 .

[118]  P. Marler,et al.  Cues for Early Discrimination of Conspecific Song in the White‐Crowned Sparrow (Zonotrichia leucophrys) , 2001 .

[119]  S. Peters,et al.  Nestling growth and song repertoire size in great reed warblers: evidence for song learning as an indicator mechanism in mate choice , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[120]  P. Miller,et al.  Killer whales are capable of vocal learning , 2006, Biology Letters.

[121]  F. Nottebohm,et al.  Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[122]  D Margoliash,et al.  Auditory representation of autogenous song in the song system of white-crowned sparrows. , 1985, Proceedings of the National Academy of Sciences of the United States of America.