[en] The songbird brain is able to discriminate between the bird's own song and other conspecific songs. Determining where in the brain own- song selectivity emerges is of great importance because experience-dependent mechanisms are necessarily involved and because brain regions sensitive to self-generated vocalizations could mediate auditory feedback that is necessary for song learning and maintenance. Using functional MRI, here we show that this selectivity is present at the midbrain level. Surprisingly, the selectivity was found to be lateralized toward the right side, a finding reminiscent of the potential right lateralization of song production in zebra finches but also of own-face and own-voice recognition in human beings. These results indicate that a midbrain structure can process subtle information about the identity of a subject through experience-dependent mechanisms, challenging the classical perception of subcortical regions as primitive and nonplastic structures. They also open questions about the evolution of the cognitive skills and lateralization in vertebrates.
Disciplines :
Zoology
Author, co-author :
Poirier, Colline
Boumans, Tiny
Verhoye, Marleen
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Van der Linden, Annemie
Language :
English
Title :
Own-song recognition in the songbird auditory pathway: selectivity and lateralization.
Publication date :
2009
Journal title :
Journal of Neuroscience
ISSN :
0270-6474
eISSN :
1529-2401
Publisher :
Society for Neuroscience, Washington, United States - District of Columbia
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Bibliography
Amin N, Grace JA, Theunissen FE (2004) Neural response to bird's own song and tutor song in the zebra finch field L and caudal mesopallium.
J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190:469-489.
Bauer EE, Coleman MJ, Roberts TF, Roy A, Prather JF, Mooney R (2008) A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28:1509-1522.
Boumans T, Theunissen FE, Poirier C, Van Der Linden A (2007) Neural representation of spectral and temporal features of song in the auditory forebrain of zebra finches as revealed by functional MRI. Eur J Neurosci 26:2613-2626.
Boumans T, Gobes SM, Poirier C, Theunissen FE, Vandersmissen L, Pintjens W, Verhoye M, Bolhuis JJ, Van der Linden A (2008a) A functional MRI of auditory responses in the zebra finch forebrain reveals a hierarchical organisation based on signal strength but not selectivity. PLoS ONE 3:e3184.
Boumans T, Vignal C, Smolders A, Sijbers J, Verhoye M, Van Audekerke J, MathevonN, Van der Linden A (2008b) Functional magnetic resonance imaging in zebra finch discerns the neural substrate involved in segregation of conspecific song from background noise. J Neurophysiol 99:931-938.
Cardin JA, Schmidt MF (2004) Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J Neurophysiol 91:2148-2163.
Chew SJ, Mello C, Nottebohm F, Jarvis E, Vicario DS (1995) Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci U S A 92:3406-3410.
Cynx J (1993) Conspecific song perception in zebra finches (Taeniopygia guttata). J Comp Psychol 107:395-402.
Cynx J, Nottebohm F (1992) Role of gender, season, and familiarity in discrimination of conspecific song by zebra finches (Taeniopygia guttata). Proc Natl Acad Sci U S A 89:1368-1371.
Dave AS, Margoliash D (2000) Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290:812-816.
Dave AS, Yu AC, Margoliash D (1998) Behavioral state modulation of auditory activityin a vocal motor system. Science 282:2250-2254.
Doupe AJ, Konishi M (1991) Song-selective auditory circuits in the vocal control system of the zebra finch. Proc Natl Acad Sci U S A 88:11339-11343.
Duong TQ, Kim DS, Uurbil K, Kim SG (2001) Localized cerebral blood flow response at submillimeter columnar resolution. Proc Natl Acad Sci USA 98:10904-10909.
Floody OR, Arnold AP (1997) Song lateralization in the zebra finch. Horm Behav 31:25-34.
Fortune ES, Margoliash D (1995) Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J Comp Neurol 360:413-441.
Fu CH, Vythelingum GN, Brammer MJ, Williams SC, Amaro E Jr, Andrew CM, Yagüez L, van Haren NE, Matsumoto K, McGuire PK (2006) An fMRI study of verbal self-monitoring: neural correlates of auditory verbal feedback. Cereb Cortex 16:969-977.
Gallup GG Jr (1997) On the rise and fall of self-conception in primates. Ann N Y Acad Sci 818:72-82.
Gold JI, Knudsen EI (2000) A site of auditory experience-dependent plasticity in the neural representation of auditory space in the barn owl's inferior colliculus. J Neurosci 20:3469-3486.
Guenther FH (2006) Cortical interactions underlying the production of speech sounds. J Commun Disord 39:350-365.
Janata P, Margoliash D (1999) Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J Neurosci 19:5108-5118.
Keenan JP, Nelson A, O'Connor M, Pascual-Leone A (2001) Self-recognition and the right hemisphere. Nature 409:305.
Keller GB, Hahnloser RH (2009) Neural processing of auditory feedback during vocal practice in a songbird. Nature 457:187-190.
Kim DS, Duong TQ, Kim SG (2000) High-resolution mapping of isoorientation columns by fMRI. Nat Neurosci 3:164-169.
Leonardo A, Konishi M (1999) Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399:466-470.
Lewicki MS, Arthur BJ (1996) Hierarchical organization of auditory temporal context sensitivity. J Neurosci 16:6987-6998.
Logothetis NK, Guggenberger H, Peled S, Pauls J (1999) Functional imaging of the monkey brain. Nat Neurosci 2:555-562.
Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
Margoliash D (1997) Functional organization of forebrain pathways for song production and perception. J Neurobiol 33:671-693.
Margoliash D, Fortune ES (1992) Temporal and harmonic combination- sensitive neurons in the zebra finch's HVc. J Neurosci 12:4309-4326.
Mello CV, Vates GE, Okuhata S, Nottebohm F (1998) Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata). J Comp Neurol 395:137-160.
Nakamura K, Kawashima R, Sugiura M, Kato T, Nakamura A, Hatano K, Nagumo S, Kubota K, Fukuda H, Ito K, Kojima S (2001) Neural substrates for recognition of familiar voices: a PET study. Neuropsychologia 39:1047-1054.
Nordeen KW, Nordeen EJ (1992) Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav Neural Biol 57:58-66.
Platek SM, Loughead JW, Gur RC, Busch S, Ruparel K, Phend N, Panyavin IS, Langleben DD (2006) Neural substrates for functionally discriminating self-face from personally familiar faces. Hum Brain Mapp 27:91-98.
Poirier C, Vellema M, Verhoye M, Van Meir V, Wild JM, Balthazart J, Van Der Linden A (2008) A three-dimensional MRI atlas of the zebra finch brain in stereotaxic coordinates. Neuroimage 41:1-6.
Prather JF, Mooney R (2004) Neural correlates of learned song in the avian forebrain: simultaneous representation of self and others. Curr Opin Neurobiol 14:496-502.
Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Gün- turkün O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, et al. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
Rosa C, Lassonde M, Pinard C, Keenan JP, Belin P (2008) Investigations of hemispheric specialization of self-voice recognition. Brain Cogn 68:204-214.
Schmidt MF, Ashmore RC, Vu ET (2004) Bilateral control and interhemispheric coordination in the avian song motor system. Ann N Y Acad Sci 1016:171-186.
Schroeder CE, Lindsley RW, Specht C, Marcovici A, Smiley JF, Javitt DC (2001) Somatosensory input to auditory association cortex in the macaque monkey. J Neurophysiol 85:1322-1327.
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 98:2747-2764.
Song JH, Skoe E, Wong PC, Kraus N (2008) Plasticity in the adult human auditory brainstem following short-term linguistic training. J Cogn Neurosci 20:1892-1902.
Sugiura M, Watanabe J, Maeda Y, Matsue Y, Fukuda H, Kawashima R (2005) Cortical mechanisms ofvisual self-recognition. Neuroimage 24:143-149.
Theunissen FE, Amin N, Shaevitz SS, Woolley SM, Fremouw T, Hauber ME (2004) Song selectivity in the song system and in the auditory forebrain. Ann N Y Acad Sci 1016:222-245.
Tourville JA, Reilly KJ, Guenther FH (2008) Neural mechanisms underlying auditory feedback control of speech. Neuroimage 39:1429-1443.
Toyomura A, Koyama S, Miyamaoto T, Terao A, Omori T, Murohashi H, Kuriki S (2007) Neural correlates of auditory feedback control in human. Neuroscience 146:499-503.
Uddin LQ, Iacoboni M, Lange C, Keenan JP (2007) The selfand social cognition: the role ofcortical midline structures and mirror neurons. Trends Cogn Sci 11:153-157.
Van Meir V, Boumans T, De GroofG, Van Audekerke J, Smolders A, Scheun- ders P, Sijbers J, Verhoye M, Balthazart J, Van der Linden A (2005) Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks. Neuroimage 25:1242-1255.
Voss HU, Tabelow K, Polzehl J, Tchernichovski O, Maul KK, Salgado-Commissariat D, Ballon D, Helekar SA (2007) Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography. Proc Natl Acad Sci U S A 104:10667-10672.
Wild JM (2004) Functional neuroanatomy of the sensorimotor control of singing. Ann N Y Acad Sci 1016:438-462.
Williams H, Nottebohm F (1985) Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. Science 229:279-282.
Williams H, Crane LA, Hale TK, Esposito MA, Nottebohm F (1992) Right-side dominance for song control in the zebra finch. J Neurobiol 23:1006-1020.
Woolley SM, Casseday JH (2005) Processing of modulated sounds in the zebra finch auditory midbrain: responses to noise, frequency sweeps, and sinusoidal amplitude modulations. J Neurophysiol 94:1143-1157.
Woolley SM, Fremouw TE, Hsu A, Theunissen FE (2005) Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8:1371-1379.
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