Learned Birdsong and the Neurobiology of Human Language

Abstract: Vocal learning, the substrate for human language, is a rare trait found to date in only three distantly related groups of mammals (humans, bats, and cetaceans) and three distantly related groups of birds (parrots, hummingbirds, and songbirds). Brain pathways for vocal learning have been studied in the three bird groups and in humans. Here I present a hypothesis on the relationships and evolution of brain pathways for vocal learning among birds and humans. The three vocal learning bird groups each appear to have seven similar but not identical cerebral vocal nuclei distributed into two vocal pathways, one posterior and one anterior. Humans also appear to have a posterior vocal pathway, which includes projections from the face motor cortex to brainstem vocal lower motor neurons, and an anterior vocal pathway, which includes a strip of premotor cortex, the anterior basal ganglia, and the anterior thalamus. These vocal pathways are not found in vocal non‐learning birds or mammals, but are similar to brain pathways used for other types of learning. Thus, I argue that if vocal learning evolved independently among birds and humans, then it did so under strong genetic constraints of a pre‐existing basic neural network of the vertebrate brain.

[1]  M. E. Raichle,et al.  Right Anterior Prefrontal Cortex Activation during Semantic Monitoring and Working Memory , 1998, NeuroImage.

[2]  Gregory F Ball,et al.  Neural bases of song preferences in female zebra finches (Taeniopygia guttata) , 1998, Neuroreport.

[3]  O. Creutzfeldt,et al.  Neuronal activity in the human lateral temporal lobe , 1989, Experimental Brain Research.

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

[5]  J. Mohr,et al.  Broca’s Area and Broca’s Aphasia (1976) , 2006 .

[6]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

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

[8]  P. Broca Nouvelle observation d’aphémie produite par une lésion de la moitié postérieure des deuxième et troisième circonvolutions frontales , 1861 .

[9]  C. Mello,et al.  Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  H. Karten,et al.  Connections of the auditory forebrain in the pigeon (columba livia) , 1993, The Journal of comparative neurology.

[11]  K. Okanoya,et al.  Partial lesions in the anterior forebrain pathway affect song production in adult Bengalese finches , 2001, Neuroreport.

[12]  P. D. Perepelkin,et al.  Neurophysiological codes of words in subcortical structures of the human brain , 1979, Brain and Language.

[13]  Nielsen Jm,et al.  Bilateral lesions of the anterior cingulate gyri; report of case. , 1951 .

[14]  C. Larson On the relation of PAG neurons to laryngeal and respiratory muscles during vocalization in the monkey , 1991, Brain Research.

[15]  R. Bandler,et al.  Brain stem integration of vocalization: role of the nucleus retroambigualis. , 1995, Journal of neurophysiology.

[16]  S. Bottjer,et al.  Circuits, hormones, and learning: vocal behavior in songbirds. , 1997, Journal of neurobiology.

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

[18]  N. Geschwind Specializations of the human brain. , 1979, Scientific American.

[19]  G. E. Vates,et al.  Feedback circuitry within a song-learning pathway. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Catherine E. Carr,et al.  The Central Auditory System of Reptiles and Birds , 2000 .

[21]  J. Talairach,et al.  Hemispheric lateralization of motor and speech functions after early brain lesion: Study of 73 epileptic patients with intracarotid amytal test , 1988, Neuropsychologia.

[22]  A. Álvarez-Buylla,et al.  Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. , 1997, Journal of neurobiology.

[23]  J. Winer,et al.  Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons , 1999, The Journal of comparative neurology.

[24]  P. Lieberman On the nature and evolution of the neural bases of human language. , 2002, American journal of physical anthropology.

[25]  J. S. McCasland,et al.  Neuronal control of bird song production , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[27]  M. Alexander,et al.  Correlations of subcortical CT lesion sites and aphasia profiles. , 1987, Brain : a journal of neurology.

[28]  J. Cummings Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[29]  G. McCarthy,et al.  Functional organization of human supplementary motor cortex studied by electrical stimulation , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  M. Glickstein,et al.  Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei , 1985, The Journal of comparative neurology.

[31]  C. Capaday,et al.  Intracortical connections between motor cortical zones controlling antagonistic muscles in the cat: a combined anatomical and physiological study , 1998, Experimental Brain Research.

[32]  A. Damasio,et al.  Nonhaemorrhagic thalamic infarction. Clinical, neuropsychological and electrophysiological findings in four anatomical groups defined by computerized tomography. , 1985, Brain : a journal of neurology.

[33]  Jessica A. Cardin,et al.  Song system auditory responses are stable and highly tuned during sedation, rapidly modulated and unselective during wakefulness, and suppressed by arousal. , 2003, Journal of neurophysiology.

[34]  D. Margoliash,et al.  Neuronal populations and single cells representing learned auditory objects , 2003, Nature.

[35]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[36]  P. Lavenex Lesions in the budgerigar vocal control nucleus NLc affect production, but not memory, of English words and natural vocalizations , 2000, The Journal of comparative neurology.

[37]  H. Karten,et al.  The Origins of Neocortex: Connections and Lamination as Distinct Events in Evolution , 1989, Journal of Cognitive Neuroscience.

[38]  B. Mazoyer,et al.  A Common Language Network for Comprehension and Production: A Contribution to the Definition of Language Epicenters with PET , 2000, NeuroImage.

[39]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[40]  S. Bottjer,et al.  An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch , 2004, The Journal of comparative neurology.

[41]  A. Russell,et al.  On the Evolution of Feathers from an Aerodynamic and Constructional View Point , 2000 .

[42]  C. Larson,et al.  Modification in activity of medullary respiratory-related neurons for vocalization and swallowing. , 1994, Journal of neurophysiology.

[43]  Marc F. Schmidt,et al.  Interhemispheric Coordination of Premotor Neural Activity during Singing in Adult Zebra Finches , 1998, The Journal of Neuroscience.

[44]  K Ugurbil,et al.  Functional magnetic resonance imaging of Broca's area during internal speech. , 1993, Neuroreport.

[45]  Erich D. Jarvis,et al.  Brains and birdsong , 2004 .

[46]  Eliot A. Brenowitz,et al.  Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. , 2000, Journal of neurobiology.

[47]  P. Mu¨ller-Preuss,et al.  Inhibition of auditory cortical neurons during phonation , 1981, Brain Research.

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

[49]  G A Ojemann,et al.  Language-related potentials specific to human language cortex. , 1981, Science.

[50]  W. Grodd,et al.  Differential Contributions of Motor Cortex, Basal Ganglia, and Cerebellum to Speech Motor Control: Effects of Syllable Repetition Rate Evaluated by fMRI , 2001, NeuroImage.

[51]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[52]  P. Lieberman Human Language and Our Reptilian Brain: The Subcortical Bases of Speech, Syntax, and Thought , 2001, Perspectives in biology and medicine.

[53]  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.

[54]  Fernando Nottebohm,et al.  The Origins of Vocal Learning , 1972, The American Naturalist.

[55]  Estrella Rausell,et al.  Area 3a in the cat II. Projections to the motor cortex and their relations to other corticocortical connections , 1992, The Journal of comparative neurology.

[56]  Minmin Luo,et al.  An Avian Basal Ganglia Pathway Essential for Vocal Learning Forms a Closed Topographic Loop , 2001, The Journal of Neuroscience.

[57]  D. Vicario,et al.  Brain pathways for learned and unlearned vocalizations differ in zebra finches , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  J. Wild,et al.  Reciprocal connections between primary and secondary auditory pathways in the telencephalon of the budgerigar (Melopsittacus undulatus) , 1997, Brain Research.

[59]  Richard R. Fay,et al.  The Mammalian Auditory Pathway: Neuroanatomy , 1992, Springer Handbook of Auditory Research.

[60]  Michael A Farries,et al.  Complementary ‘bottom-up’ and ‘top-down’ approaches to basal ganglia function , 2000, Current Opinion in Neurobiology.

[61]  E. Rouiller,et al.  Mapping of c-fos expression elicited by pure tones stimulation in the auditory pathways of the rat, with emphasis on the cochlear nucleus , 1992, Neuroscience Letters.

[62]  S. Bottjer,et al.  Lesions of a telencephalic nucleus in male zebra finches: Influences on vocal behavior in juveniles and adults. , 2001, Journal of neurobiology.

[63]  Y. Grodzinsky The neurology of syntax: Language use without Broca's area , 2000, Behavioral and Brain Sciences.

[64]  S. Bookheimer,et al.  Activation of language cortex with automatic speech tasks , 2000, Neurology.

[65]  M. Schmidt,et al.  Comparative approaches to avian song system function: insights into auditory and motor processing , 2002, Journal of Comparative Physiology A.

[66]  Jon E. Ahlquist,et al.  Phylogeny and Classification of the Birds: A Study in Molecular Evolution , 1991 .

[67]  A. Doupe,et al.  Singing-Related Neural Activity in a Dorsal Forebrain–Basal Ganglia Circuit of Adult Zebra Finches , 1999, The Journal of Neuroscience.

[68]  O. W. Henson,et al.  The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus , 1990, Brain Research Reviews.

[69]  S. Brauth,et al.  Comparison of the effects of lesions in nucleus basalis and field 'L' on vocal learning and performance in the budgerigar (Melopsittacus undulatus). , 1994, Brain, behavior and evolution.

[70]  P. Marler,et al.  Vervet monkey alarm calls: Semantic communication in a free-ranging primate , 1980, Animal Behaviour.

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

[72]  S. Brauth,et al.  Auditory Pathways in the Budgerigar , 1987 .

[73]  Fernando Nottebohm,et al.  Reafferent thalamo‐“cortical” loops in the song system of oscine songbirds , 1997, The Journal of comparative neurology.

[74]  E J Auerbach,et al.  Activity in the paracingulate and cingulate sulci during word generation: an fMRI study of functional anatomy. , 1999, Cerebral cortex.

[75]  H. Kuypers,et al.  Distribution of corticospinal neurons with collaterals to the lower brain stem reticular formation in monkey (Macaca fascicularis) , 2004, Experimental Brain Research.

[76]  F. Nottebohm,et al.  Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  S. Durand,et al.  Functional anatomy of forebrain auditory pathways in the budgerigar (Melopsittacus undulatus). , 1994, Brain, behavior and evolution.

[78]  E. Nordeen,et al.  Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. , 1990, Behavioral and neural biology.

[79]  R. Wiley,et al.  Physical constraints on acoustic communication in the atmosphere: Implications for the evolution of animal vocalizations , 1978, Behavioral Ecology and Sociobiology.

[80]  M Freedman,et al.  Anatomic basis of transcortical motor aphasia , 1984, Neurology.

[81]  Johan J. Bolhuis,et al.  Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches , 2001, The European journal of neuroscience.

[82]  H. Kuypers CORTICOBULBAR CONNEXIONS TO THE PONS AND LOWER BRAIN-STEM IN MAN , 1958 .

[83]  A R Damasio,et al.  Aphasia with nonhemorrhagic lesions in the basal ganglia and internal capsule. , 1982, Archives of neurology.

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

[85]  R. Dooling,et al.  Auditory Pathways in the Budgerigar (Part 1 of 2) , 1987 .

[86]  O. Creutzfeldt,et al.  Neuronal activity in the human lateral temporal lobe , 2004, Experimental Brain Research.

[87]  J. Houk,et al.  Network models of the basal ganglia , 1997, Current Opinion in Neurobiology.

[88]  D. Margoliash,et al.  Song replay during sleep and computational rules for sensorimotor vocal learning. , 2000, Science.

[89]  M. Gahr Neural song control system of hummingbirds: Comparison to swifts, vocal learning (Songbirds) and nonlearning (Suboscines) passerines, and vocal learning (Budgerigars) and nonlearning (Dove, owl, gull, quail, chicken) nonpasserines , 2000, The Journal of comparative neurology.

[90]  U. Jürgens,et al.  The Effects of Deep-Reaching Lesions in the Cortical Face Area on Phonation a Combined Case Report and Experimental Monkey Study , 1982, Cortex.

[91]  P. Marler,et al.  Animal Communication Signals , 1967, Science.

[92]  M. Novacek,et al.  Mammalian phylogeny: Genes and supertrees , 2001, Current Biology.

[93]  Kazuo Okanoya,et al.  Lesion of a higher‐order song nucleus disrupts phrase level complexity in Bengalese finches , 2000, Neuroreport.

[94]  T. J. Seller Midbrain vocalization centres in birds , 1981, Trends in Neurosciences.

[95]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[96]  Lucie Hertz-Pannier,et al.  Late plasticity for language in a child's non-dominant hemisphere: a pre- and post-surgery fMRI study. , 2002, Brain : a journal of neurology.

[97]  D. Poeppel A Critical Review of PET Studies of Phonological Processing , 1996, Brain and Language.

[98]  M. Farries The Oscine Song System Considered in the Context of the Avian Brain: Lessons Learned from Comparative Neurobiology , 2002, Brain, Behavior and Evolution.

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

[100]  U. Jürgens,et al.  The role of the periaqueductal grey in vocal behaviour , 1994, Behavioural Brain Research.

[101]  E. Jarvis,et al.  Molecular mapping of brain areas involved in parrot vocal communication , 2000, The Journal of comparative neurology.

[102]  H. Karten,et al.  Homology and evolutionary origins of the 'neocortex'. , 1991, Brain, behavior and evolution.

[103]  G. Striedter,et al.  The vocal control pathways in budgerigars differ from those in songbirds , 1994, The Journal of comparative neurology.

[104]  J. Wild,et al.  Neural pathways for the control of birdsong production. , 1997, Journal of neurobiology.

[105]  H. Scheich,et al.  Connectivity of the auditory forebrain nuclei in the Guinea Fowl (Numida meleagris) , 1979, Cell and Tissue Research.

[106]  R. Strub,et al.  Frontal lobe syndrome in a patient with bilateral globus pallidus lesions. , 1989, Archives of neurology.

[107]  J. Leicester Central deafness and subcortical motor aphasia , 1980, Brain and Language.

[108]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[109]  N. Dronkers A new brain region for coordinating speech articulation , 1996, Nature.

[110]  S. Petersen,et al.  Comparison of Brain Activation during Word Retrieval Done Silently and Aloud Using fMRI , 2000, Brain and Cognition.

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

[112]  G. Striedter,et al.  Brain lesions that impair vocal imitation in adult budgerigars. , 2002, Journal of neurobiology.

[113]  E. Valenstein Nonlanguage disorders of speech reflect complex neurologic apparatus. , 1975, Geriatrics.

[114]  H. Kornhuber,et al.  Observations on regional cerebral blood flow in cortical and subcortical structures during language production in normal man , 1985, Brain and Language.

[115]  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.

[116]  Uwe Jürgens,et al.  Neuronal Control of Vocal Production in Non-Human and Human Primates , 1995 .

[117]  A. Hartemink,et al.  A framework for integrating the songbird brain , 2002, Journal of Comparative Physiology A.

[118]  U. Jürgens,et al.  Cortical lesion effects and vocalization in the squirrel monkey , 1982, Brain Research.

[119]  J. Winer,et al.  Layer V in cat primary auditory cortex (AI): Cellular architecture and identification of projection neurons , 2001, The Journal of comparative neurology.

[120]  A Keller,et al.  The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. , 1993, Journal of neurophysiology.

[121]  A. Rubens Aphasia With Infarction in the Territory of the Anterior Cerebral Artery , 1975, Cortex.

[122]  F. Sheldon,et al.  Avian vocalizations and phylogenetic signal. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[123]  E. Jarvis,et al.  Differential expression of glutamate receptors in avian neural pathways for learned vocalization , 2004, The Journal of comparative neurology.

[124]  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.

[125]  Peter Marler,et al.  Vocal communication in the domestic chicken: I. Does a sender communicate information about the quality of a food referent to a receiver? , 1986, Animal Behaviour.

[126]  David J Perkel,et al.  Songbirds and the Revised Avian Brain Nomenclature , 2004, Annals of the New York Academy of Sciences.

[127]  Mark D. Johnson,et al.  The Role of the Human Thalamus in Language and Memory: Evidence from Electrophysiological Studies , 2000, Brain and Cognition.

[128]  Sidarta Ribeiro,et al.  Behaviourally driven gene expression reveals song nuclei in hummingbird brain , 2000, Nature.

[129]  D. Fitzpatrick The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. , 1996, Cerebral cortex.

[130]  G. Ojemann Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[131]  H. Kuypers Some projections from the peri‐central cortex to the pons and lower brain stem in monkey and chimpanzee , 1958, The Journal of comparative neurology.

[132]  F. Nottebohm,et al.  Context determines the sex appeal of male zebra finch song , 1998, Animal Behaviour.

[133]  M. Biederman-Thorson Auditory responses of units in the ovoid nucleus and cerebrum (field L) of the ring dove. , 1970, Brain research.

[134]  S. Petersen,et al.  Frontal cortex contributes to human memory formation , 1999, Nature Neuroscience.

[135]  E I Knudsen,et al.  Auditory tuning for spatial cues in the barn owl basal ganglia. , 1994, Journal of neurophysiology.

[136]  M. Novacek,et al.  Mammalian phytogeny: shaking the tree , 1992, Nature.

[137]  Richard Hans Robert Hahnloser,et al.  An ultra-sparse code underliesthe generation of neural sequences in a songbird , 2002, Nature.

[138]  F. Nottebohm,et al.  Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway. , 1998, Journal of neurobiology.

[139]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[140]  D. Vicario,et al.  Song presentation induces gene expression in the songbird forebrain. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[141]  A. Esposito,et al.  Complete mutism after midbrain periaqueductal gray lesion. , 1999, Neuroreport.

[142]  F. Nottebohm,et al.  Motor-driven gene expression. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[143]  S. Bottjer,et al.  Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches , 1997, The Journal of comparative neurology.

[144]  C. Eagleton,et al.  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) , 1997, The Journal of comparative neurology.

[145]  Kisou Kubota,et al.  Cortical projection to hand-arm motor area from post-arcuate area in macaque monkeys: A histological study of retrograde transport of horseradish peroxidase , 1979, Neuroscience Letters.

[146]  G. Ojemann The neurobiology of language and verbal memory: observations from awake neurosurgery. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[147]  D. Benson,et al.  Aphasia: A Clinical Perspective , 1996 .

[148]  A. Laverghetta,et al.  Differential morphology of pyramidal tract‐type and intratelencephalically projecting‐type corticostriatal neurons and their intrastriatal terminals in rats , 2003, The Journal of comparative neurology.

[149]  K. Heilman,et al.  Disruption of automatic speech following a right basal ganglia lesion , 1993, Neurology.

[150]  J. Trojanowski,et al.  Corticothalamic neurons and thalamocortical terminal fields: An investigation in rat using horseradish peroxidase and autoradiography , 1975, Brain Research.

[151]  Y. Cohen,et al.  Representation of frequency in the primary auditory field of the barn owl forebrain. , 1996, Journal of neurophysiology.

[152]  S. Durand,et al.  Vocal control pathways through the anterior forebrain of a parrot (Melopsittacus undulatus) , 1997, The Journal of comparative neurology.

[153]  F. Nottebohm,et al.  Associative learning and stimulus novelty influence the song-induced expression of an immediate early gene in the canary forebrain. , 1995, Learning & memory.

[154]  C. Mello,et al.  Differential induction of the ZENK gene in the avian forebrain and song control circuit after metrazole-induced depolarization. , 1995, Journal of neurobiology.

[155]  D. Margoliash,et al.  Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata) , 1995, The Journal of comparative neurology.

[156]  Hoi-Chung Leung,et al.  Frontal activations associated with accessing and evaluating information in working memory: an fMRI study , 2003, NeuroImage.

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

[158]  S Jonas,et al.  The supplementary motor region and speech emission. , 1981, Journal of communication disorders.

[159]  P. Slater,et al.  Bird Song: Biological Themes and Variations , 1995 .

[160]  G. Ojemann Neurophysiological codes of words in subcortical structures of the human brain, by Bechtereva, Bundzen, Gogolitsin, Malyshev, and Perepelkin , 1979, Brain and Language.

[161]  H. Williams,et al.  Song learning in birds: the relation between perception and production. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[162]  E. Friauf Tonotopic Order in the Adult and Developing Auditory System of the Rat as Shown by c‐fos Immunocytochemistry , 1992, The European journal of neuroscience.

[163]  R. Zann The Zebra Finch: A Synthesis of Field and Laboratory Studies , 1996 .

[164]  F. Nottebohm,et al.  For Whom The Bird Sings Context-Dependent Gene Expression , 1998, Neuron.

[165]  Alan C. Evans,et al.  Left putaminal activation when speaking a second language: evidence from PET. , 1994, Neuroreport.

[166]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[167]  R W BARRIS,et al.  Bilateral Anterior Cingulate Gyrus Lesions , 1953, Neurology.

[168]  A. Doupe,et al.  Social context modulates singing-related neural activity in the songbird forebrain , 1999, Nature Neuroscience.

[169]  J. Wild,et al.  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, columbia livia , 1994, The Journal of comparative neurology.

[170]  Fernando Nottebohm,et al.  Descending auditory pathways in the adult male zebra finch (Taeniopygia Guttata) , 1998, The Journal of comparative neurology.

[171]  U. Jürgens,et al.  Neuronal activity in the periaqueductal gray and bordering structures during vocal communication in the squirrel monkey , 2004, Neuroscience.