Connections of the auditory brainstem in a songbird, Taeniopygia guttata. I. projections of nucleus angularis and nucleus laminaris to the auditory torus

Journal of Comparative Neurology

Volumn 518, Issue 11, 2010, Pages 2109-2134

  Krützfeldt, Nils O E ^a   Logerot, Priscilla ^a   Kubke, M Fabiana ^a   Wild, J Martin ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Avian; Central nucleus of inferior colliculus; Cochlear nuclei; MLd; Zebra finch

Indexed keywords

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; AUDITORY STIMULATION; BRAIN STEM; COCHLEAR NUCLEUS; FINCH; INFERIOR COLLICULUS; MAGNOCELLULAR NUCLEUS; MAMMAL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; SONGBIRD; TELENCEPHALON; THALAMUS INTRALAMINAR NUCLEUS;

ANIMALS; AUDITORY PATHWAYS; BRAIN STEM; COCHLEAR NUCLEUS; FINCHES; HUMANS; INFERIOR COLLICULI; MALE; STAINING AND LABELING;

EID: 77952191641     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22334     Document Type: Article

References (118)

1. Adolphs R. 1993. Acetylcholinesterase staining differentiates functionally distinct auditory pathways in the barn owl. J Comp Neurol 329: 365-377. (Pubitemid 23078231)
2. Alain C, Arnott SR, Hevenor S, Graham, S, Grady CL. 2001. "What" and "where" in the human auditory system. Proc Natl Acad Sci U S A 98: 12301-12306.
3. Anderson LA, Malmierca MS, Wallace MN, Palmer AR. 2006. Evidence for a direct, short latency projection from the dorsal cochlear nucleus to the auditory thalamus in the guinea pig. Eur J Neurosci 24: 491-498.
4. Anderson LA, Izquierdo MA, Antunes FM. 2009. A monosynaptic pathway from dorsal cochlear nucleus to auditory cortex in rat. Neuroreport 20: 462-466.
5. Arends JJ. 1981. Sensory and motor aspects of the trigeminal system in the mallard (Anas Platyrhynchos L.). PhD Thesis. Leiden, Netherlands: University of Leiden.
6. Arends JJ, Zeigler HP. 1986. Anatomical identification of an auditory pathway from a nucleus of the lateral lemniscal system to the frontal telencephalon (nucleus basalis) of the pigeon. Brain Res 398: 375-381.
7. Boord RL. 1968. Ascending projections of the primary cochlear nuclei and nucleus laminaris in the pigeon. J Comp Neurol 133: 523-541.
8. Boord RL, Rasmussen GL. 1963. Projection of the cochlear and lagenar nerves on the cochlear nuclei of the pigeon. J Comp Neurol 120: 463-475.
9. Braun K, Scheich H, Schachner M, Heizmann CW. 1985. Distribution of parvalbumin, cytochrome oxidase activity and 14C-2-deoxyglueose uptake in the brain of the zebra finch I. Auditory and vocal motor systems. Cell Tissue Res 240: 101-115.
10. Braun K, Scheich H, Heizmann CW, Hunziker W. 1991. Parvalbumin and calbindin-D28K immunoreactivity as developmental markers of auditory and vocal motor nuclei of the zebra finch. Neuroscience 40: 853-869.
11. Calford MB. 1988. Constraints on the coding of sound frequency imposed by the avian interaural canal. J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 162: 491-502.
12. Calford MB, Wise LZ, Pettigrew JD. 1985. Coding of sound location and frequency in the auditory midbrain of diurnal birds of prey, families accipitridae and falconidae. J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 157: 149-160.
13. Cant NB. 2005. Projections from the cochlear nuclear complex to the inferior colliculus. In: Winer JA, Schreiner CE, editors. The inferior colliculus. New York: Springer, p 115-131.
14. Cant NB, Benson CG. 2003. Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60: 457-474.
15. Cant NB, Benson CG. 2008. Organization of the inferior colliculus of the gerbil: projections from the cochlear nucleus. Neuroscience 154: 206-217.
16. Carr CE, Boudreau RE. 1991. Central projections of auditory nerve fibers in the barn owl. J Comp Neurol 314: 306-318.
17. Carr CE, Konishi M. 1990. A circuit for detection of interaural time differences in the brainstem of the bam owl. J Neurosci 10: 3227-3246.
18. Carr CE, Fujita I, Konishi M. 1989. Distribution of GABAergic neurons and terminals in the auditory system of the barn owl. J Comp Neurol 286: 190-207. (Pubitemid 19220591)
19. Casseday JH, Covey E. 1996. A neuroethological theory of the operation of the inferior colliculus. Brain Behav Evol 47: 311-336. (Pubitemid 126464502)
20. Celio MR, Baier W, Scharer L, de Viragh PA, Gerday C. 1988. Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9 :81-86.
21. Clack JA. 1997. The evolution of tetrapod ears and the fossil record. Brain Behav Evol 50: 198-212.
22. Coleman MJ, Mooney R. 2004. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J Neurosci 24: 7251-7265. (Pubitemid 39100695)
23. Coles RB, Aitken LM. 1979. The response properties of auditory neurons in the midbrain of the domestic fowl (Callus gallus) to monaural and binaural stimuli. J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 134: 241-251.
24. Conlee JW, Parks TN. 1986. Origin of ascending auditory projections to the nucleus mesencephalicus lateralis pars dorsalis in the chicken. Brain Res 367: 96-113.
25. Correia MJ, Eden AR, Westlund KN, Coulter JD. 1982. Organization of ascending auditory pathways in the pigeon (Columba livia) as determined by autoradiographic methods. Brain Res 234: 205-212.
26. Covey E, Carr CE. 2005. The auditory midbrain in bats and birds. In: Winer JA, Schreiner CE, editors. The inferior colliculus. New York: Springer, p 493-536.
27. Cynx J, Von Rad U. 2001. Immediate and transitory effects of delayed auditory feedback on bird song production. Anim Behav 62: 305-312. (Pubitemid 32792876)
28. Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E. 2008. 'Where' and 'what' in the whisker sensorimotor system. Nat Rev Neurosci 9: 601-612.
29. 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. (Pubitemid 21916036)
30. 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.
31. Fukui I, Ohmori H. 2003. Nucleus angularis of the chicken: developmental changes in membrane excitability and morphology of neurons. J Physiol 548: 219-232. (Pubitemid 36410810)
32. Grace JA, Amin N, Singh NC, Theunissen FE. 2003. Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89: 472-487. (Pubitemid 36134037)
33. Grothe B. 2003. New roles for synaptic inhibition in sound localization. Nate Rev Neurosci 4: 540-550. (Pubitemid 37271365)
34. Gurney ME. 1981. Hormonal control of cell form and number in the zebra finch song system. J Neurosci 1: 658-673.
35. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763-1768. (Pubitemid 351931288)
36. Häusler UH, Sullivan WE, Soares D, Carr CE. 1999. A morphological study of the cochlear nuclei of the pigeon (Columba livia). Brain Behav Evol 54: 290-302. (Pubitemid 30041387)
37. Hsu A, Woolley SM, Fremouw TE, Theunissen FE. 2004. Modulation power and phase spectrum of natural sounds enhance neural encoding performed by single auditory neurons. J Neurosci 24: 9201-9211. (Pubitemid 39372264)
38. Hyson RL. 2005. The analysis of interaural time differences in the chick brain stem. Physiol Behav 86: 297-305.
39. 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. (Pubitemid 29270145)
40. Jeffress LA. 1948. A place theory of sound localization. J Comp Physiol Psychol 41: 35-39.
41. Jhaveri S, Morest DK. 1982. Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: a light and electron microscope study. Neuroscience 7: 809-836. (Pubitemid 12122238)
42. Karten HJ. 1967. The organization of the ascending auditory pathway in the pigeon (Columba livia). I. Diencephalic projections of the inferior colliculus (nucleus mesencephali lateralis, pars dorsalis). Brain Res 6: 409-427.
43. Karten HJ. 1968. The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res 11: 134-153.
44. Karten HJ, Hodos W. 1967. A stereotaxic atlas of the brain of the pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.
45. Kelley DB, Nottebohm F. 1979. Projections of a telencephalic auditory nucleus-field L-in the canary. J Comp Neurol 183: 455-469.
46. Klump GM. 2000. Sound localization in birds. In: Dooling RJ, Fay RR, Popper AN, editors. Comparative hearing: birds and reptiles, vol.13. New York: Springer, p 380.
47. Klump GM, Windt W, Curio E. 1986. The great tit's (Parus major) auditory resolution in azimuth. J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 158: 383-390.
48. Knudsen El. 1983. Subdivisions of the inferior colliculus in the barn owl (Tyto alba). J Comp Neurol 218: 174-186.
49. Knudsen El. 2002. Instructed learning in the auditory localization pathway of the barn owl. Nature 417: 322-328.
50. Knudsen El, Konishi M. 1978. Space and frequency are represented separately in auditory midbrain of the owl. J Neurophysiol 41: 870-884. (Pubitemid 8392563)
51. Knudsen El, Knudsen PF. 1983. Space-mapped auditory projections from the inferior colliculus to the optic tectum in the bam owl (Tyto alba). J Comp Neurol 218: 187-196.
52. Knudsen El, Blasdel GG, Konishi M. 1979. Sound localization by the barn owl (Tyto alba) measured with the search coil technique. J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 133: 1-11.
53. Konishi M. 1965. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z Tierpsychol 22: 770-783.
54. Konishi M. 1970. Comparative neurophysiological studies of hearing and vocalizations in songbirds. Z vergl Physiol 66: 257-272.
55. Konishi M. 1995. Neural mechanisms of auditory image formation. In: Gazzaniga MS, editor. The cognitive neurosciences. Boston: MIT Press, p 269-277.
56. Konishi M. 2003. Coding of auditory space. Annu Rev Neurosci 26: 31-55.
57. Köppl C. 1994. Auditory nerve terminals in the cochlear nucleus magnocellularis: differences between low and high frequencies. J Comp Neurol 339: 438-446. (Pubitemid 24012953)
58. Köppl C. 2001. Tonotopic projections of the auditory nerve to the cochlear nucleus angularis in the barn owl. J Assoc Res Otolaryngol 2: 41-53. (Pubitemid 32591891)
59. Köppl C, Carr CE. 2003. Computational diversity in the cochlear nucleus angularis of the barn owl. J Neurophysiol 89: 2313-2329. (Pubitemid 36444283)
60. Krützfeldt NOE, Logerot P, Kubke MF, Wild JM. 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: 2135-2148.
61. Kubke MF, Gauger B, Basu L, Wagner H, Carr CE. 1999. Development of calretinin immunoreactivity in the brainstem auditory nuclei of the bam owl (Tyto alba). J Comp Neurol 415: 189-203. (Pubitemid 29519876)
62. Kubke MF, Ross JM, Wild JM. 2004. Vagal innervation of the air sacs in a songbird, Taenopygia guttata. J Anat 204: 283-292.
63. Larsen ON, Dooling RJ, Michelsen. 2006. The role of pressure difference reception in the directional hearing of budgerigars (Melopsittacus undulatus). J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 192: 1063-1072.
64. Leibler LM. 1975. Monaural and binaural pathways in the ascending auditory system of the pigeon. PhD Thesis. Cambridge, MA: Massachusetts Institute of Technology.
65. Leonardo A, Konishi M. 1999. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399: 466-470. (Pubitemid 29258851)
66. Lewald J. 1990. Neural mechanisms of directional hearing in the pigeon. Exp Brain Res 82: 423-436. (Pubitemid 20378101)
67. Logerot P, Wild JM, Kubke MF. 2009. Auditory processing of conspecific vocalizations in the auditory midbrain of the zebra finch. Paper presented at the Australasian Winter Conference on Brain Research, Queenstown, New Zealand, August 29-September 2.
68. Lombardino AJ, Nottebohm F. 2000. Age at deafening affects the stability of learned song in adult male zebra finches. J Neurosci 20: 5054-5064. (Pubitemid 30421709)
69. Malmierca MS, Merchan MA, Henkel CK, Oliver DL. 2002. Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci 22: 10891-10897.
70. Malmierca MS, Saint Marie RL, Merchan MA, Oliver DL. 2005. Laminar inputs from dorsal cochlear nucleus and ventral cochlear nucleus to the central nucleus of the inferior colliculus: two patterns of convergence. Neuroscience 136: 883-894.
71. Marler P, Waser MS. 1977. Role of auditory feedback in canary song development. J Comp Physiol Psychol 91: 8-16. (Pubitemid 8187243)
72. Masino T, Knudsen El. 1992. Anatomical pathways from the optic tectum to the spinal cord subserving orienting movements in the bam owl. Exp Brain Res 92: 194-208. (Pubitemid 23018029)
73. 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. (Pubitemid 28234594)
74. Nelson BS, Stoddard PK. 1998. Accuracy of auditory distance and azimuth perception by a passerine bird in natural habitat. Anim Behav 56: 467-477.
75. Nelson BS, Suthers RA. 2004. Sound localization in a small passerine bird: discrimination of azimuth as a function of head orientation and sound frequency. J Exp Biol 207(Pt 23): 4121-4133.
76. 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.
77. Nottebohm F, Stokes TM, Leonard CM. 1976. Central control of song in the canary, Serinus canarius. J Comp Neurol 165: 457-486.
78. Okanoya K, Yamaguchi A. 1997. Adult Bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax. J Neurobiol 33: 343-356. (Pubitemid 27411216)
79. Oliver DL. 2005. Neuronal organization in the inferior colliculus. In: Winer JA, Schreiner CE, editors. The inferior colliculus. New York: Springer, p 69-114.
80. Osen KK. 1972. Projection of the cochlear nuclei on the inferior colliculus in the cat. J Comp Neurol 144: 355-372.
81. Park TJ, Dooling RJ. 1991. Sound localization in small birds: absolute localization in azimuth. J Comp Psychol 105: 125-133.
82. Parks TN, Rubel EW. 1975. Organization and development of brain stem auditory nuclei of the chicken: organization of projections from n. magnocellularis to n. laminaris. J Comp Neurol 164: 435-448.
83. Payne RS. 1971. Acoustic location of prey by barn owls (Tyto alba). J Exp Biol 54: 535-573.
84. Poirier C, Boumans T, Verhoye M, Balthazart J, Van der Linden A. 2009. Own-song recognition in the songbird auditory pathway. J Neurosci 29: 2252-2258.
85. Puelles L, Robles C, Martinez-de-la-Torre M, Martinez S. 1994. New subdivision schema for the avian torus semicircularis: neurochemical maps in the chick. J Comp Neurol 340: 98-125. (Pubitemid 24036461)
86. Puelles L, Martinez-de-la-Torre M, Paxinos G, Watson C, Martinez S. 2007. The chick brain in stereotaxic coordinates. An atlas featuring neuromeric subdivisions and mammalian homologies. Amsterdam: Elsevier, Academic Press.
87. Sachs MB, Sinnott JM. 1978. Responses to tones of single cells in nucleus magnocellularis and nucleus angularis of the redwing blackbird (Agelaius phoeniceus). J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 126: 347-361.
88. Scheich H, Langner G, Koch R. 1977. Coding of narrow-band and wide-band vocalizations in the auditory midbrain nucleus (MLD) of the guinea fowl (Numida meleagris). J Comp Physiol [A] Neuroethol Sens Neural Behav Physiol 117: 245-265.
89. Sen K, Theunissen FE, Doupe AJ. 2001. Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophysiol 86: 1445-1458. (Pubitemid 32847788)
90. Soares D, Carr CE. 2001. The cytoarchitecture of the nucleus angularis of the barn owl (Tyto alba). J Comp Neurol 429: 192-205.
91. Stocker SD, Simmons JR, Stometta RL, Toney GM, Guyenet PG. 2006. Water deprivation activates a glutamatergic projection from the hypothalamic paraventricular nucleus to the rostral ventrolateral medulla. J Comp Neurol 494: 673-685.
92. Sullivan WE, Konishi M. 1984. Segregation of stimulus phase and intensity coding in the cochlear nucleus of the bam owl. J Neurosci 4: 1787-1799. (Pubitemid 14055535)
93. Takahashi TT, Konishi M. 1988. Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl. J Comp Neurol 274: 190-211.
94. Takahashi TT, Carr CE, Brecha N, Konishi M. 1987. Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the bam owl. J Neurosci 7: 1843-1856. (Pubitemid 17119806)
95. Vates GE, Broome BM, Mello CV, Nottebohm F. 1996. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366: 613-642. (Pubitemid 26087298)
96. Wagner H, Takahashi T, Konishi M. 1987. Representation of interaural time difference in the central nucleus of the bam owl's inferior colliculus. J Neurosci 7: 3105-3116.
97. Wagner H, Güntürkün O, Nieder B. 2003. Anatomical markers for the subdivisions of the barn owl's inferior-collicular complex and adjacent peri- and subventricular structures. J Comp Neurol 465: 145-159. (Pubitemid 37075686)
98. Watanabe A, Aoki K. 1998. The role of auditory feedback in the maintenance of song in adult male Bengalese finches Lonchura striata var. domestica. Zool Sci 15: 837-841. (Pubitemid 128366712)
99. Watson JT, Adkins-Regan E, Whiting P, Lindstrom JM, Podleski TR. 1988. Autoradiographic localization of nicotinic acetylcholine receptors in the brain of the zebra finch (Poephila guttata). J Comp Neurol 274: 255-264.
100. Wild JM. 1987. Nuclei of the lateral lemniscus project directly to the thalamic auditory nuclei in the pigeon. Brain Res 408: 303-307.
101. Wild JM. 1993a. The avian nucleus retroambigualis: a nucleus for breathing, singing and calling. Brain Res 606: 319-324.
102. Wild JM. 1993b. Descending projections of the songbird nucleus robustus archistriatalis. J Comp Neurol 338: 225-241.
103. Wild JM. 1994. The auditory-vocal-respiratory axis in birds. Brain Behav Evol 44: 192-209.
104. Wild JM. 1995. Convergence of somatosensory and auditory projections in the avian torus semicircularis, including the central auditory nucleus. J Comp Neurol 358: 465-486.
105. Wild JM. 1997. The avian somatosensory system: the pathway from wing to Wulst in a passerine (Chloris chloris). Brain Res 759: 122-134.
106. Wild JM. 2004. Functional neuroanatomy of the sensorimotor control of singing. Ann N Y Acad Sci 1016: 438-462. (Pubitemid 38951480)
107. Wild JM. 2008. Birdsong: anatomical foundations and central mechanisms of sensorimotor integration. In: Neuroscience of birdsong. Cambridge, UK: Cambridge University Press, p 136-151.
108. Wild JM, Karten HJ, Frost BJ. 1993. Connections of the auditory forebrain in the pigeon (Columba livia). J Comp Neurol 337: 32-62.
109. Wild JM, Li D, 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: 392-413. (Pubitemid 27016647)
110. Wild JM, Williams MN, Suthers RA. 2000. Neural pathways for bilateral vocal control in songbirds. J Comp Neurol 423: 413-426.
111. Wild JM, Williams MN, Suthers RA. 2001. Parvalbumin-positive projection neurons characterise the vocal premotor path way in male, but not female, zebra finches. Brain Res 917: 235-252.
112. Wild JM, Krützfeldt NOE, Kubke MF. 2009. Afferents to the cochlear nuclei and nucleus laminaris from the ventral nucleus of the lateral lemniscus in the zebra finch (Taeniopygia guttata). Hear Res 212: 3119-3124.
113. Wild JM, Krützfeldt NOE, Kubke MF. 2010. Connections of the auditory brainstem in a songbird, Taeniopygia guttata: III. Projections of the superior olive and lateral lemniseal nuclei. J Comp Neurol 518: 2149-2167.
114. Wong-Riley M. 1979. Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res 171: 11-28.
115. Woolley SM, Casseday JH. 2004. Response properties of single neurons in the zebra finch auditory midbrain: response patterns, frequency coding, intensity coding, and spike latencies. J Neurophysiol 91: 136-151.
116. 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.
117. Woolley SM, Rubel EW. 1997. Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song. J Neurosci 17: 6380-6390.
118. Zeng SJ, Lin YT, Yang L, Zhang X-W, Zuo M-X. 2008. Comparative analysis of neurogenesis between the core and shell regions of auditory areas in the chick (Gallus gallus domesticus). Brain Res 1216: 24-37.