Early postnatal development of spontaneous and acoustically evoked discharge activity of principal cells of the medial nucleus of the trapezoid body: An in vivo study in mice

Journal of Neuroscience

Volumn 29, Issue 30, 2009, Pages 9510-9520

  Sonntag, Mandy ^a   Englitz, Bernhard ^b   Kopp Scheinpflug, Cornelia ^a   Rübsamen, Rudolf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; C57BL 6 MOUSE; CBA MOUSE; ELECTROENCEPHALOGRAM; EVOKED BRAIN STEM AUDITORY RESPONSE; HEARING; IN VIVO STUDY; MEDIAN RAPHE NUCLEUS; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TONOTOPY; TRAPEZOID BONE;

ACOUSTIC STIMULATION; ACTION POTENTIALS; AGING; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; AUDITORY PERCEPTION; AUDITORY THRESHOLD; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICROELECTRODES; NEURONS; OLIVARY NUCLEUS; REACTION TIME; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 68049122873     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1377-09.2009     Document Type: Article

References (76)

1. Berlin CI (1963) Hearing in mice via GSR audiometry. J Speech Hear Res 13:359-368.
2. Blatchley BJ, Cooper WA, Coleman JR (1987) Development of auditory brainstem response to tone pip stimuli in the rat. Brain Res 429:75-84.
3. Egorova M, Ehret G, Vartanian I, Esser KH (2001) Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics. Exp Brain Res 140:145-161.
4. Ehret G, Moffat AJ (1984) Noise masking of tone responses and critical ratios in single units of the mouse cochlear nerve and cochlear nucleus. Hear Res 14:45-57. (Pubitemid 14087433)
5. Erazo-Fischer E, Striessnig J, Taschenberger H (2007) The role of physiological afferent nerve activity during in vivo maturation of the calyx of Held synapse. J Neurosci 27:1725-1737. (Pubitemid 46280066)
6. Finck A, Schneck CD, Hartman AF (1972) Development of cochlear function in the neonate Mongolian gerbil (Meriones unguiculatus). J Comp Physiol Psychol 78:375-380.
7. Friauf E (1992) Tonotopic order in the adult and developing auditory system of the rat as shown by c-fos immunocytochemistry. Eur J Neurosci 4:798-812.
8. Futai K, Okada M, Matsuyama K, Takahashi T (2001) High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21:3342-3349. (Pubitemid 32422799)
9. Geal-Dor M, Freeman S, Li G, SohmerH (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res 69:236-242. (Pubitemid 23279615)
10. Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147-154. (Pubitemid 34121582)
11. Green JS, Sanes DH (2005) Early appearance of inhibitory input to the MNTB supports binaural processing during development. J Neurophysiol 94:3826-3835.
12. Guinan JJ Jr, Li RY (1990) Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat. Hear Res 49:321-334.
13. Guinan JJ Jr, Norris BE, Guinan SS (1972) Single auditory units in the superior olivary complex II: locations of unit categories and tonotopic organization. Int J Neurosci 4:147-166.
14. Gummer AW, Mark RF (1994) Patterned neural activity in brain stem auditory areas of a prehearing mammal, the tammar wallaby (Macropus eugenii). Neuroreport 5:685-688.
15. Harris DM, Dallos P (1984) Ontogenetic changes in frequency mapping of a mammalian ear. Science 225:741-743.
16. He DZ, Evans BN, Dallos P (1994) First appearance and development of electromotility in neonatal gerbil outer hair cells. Hear Res 78:77-90. (Pubitemid 24251594)
17. Henry KR (2004) Males lose hearing earlier in mouse models of late-onset age-related hearing loss; females lose hearing earlier in mouse models of early-onset hearing loss. Hear Res 190:141-148.
18. Henry KR, Chole RA (1980) Genotypic differences in behavioral, physiological and anatomical expressions of age-related hearing loss in the laboratory mouse. Audiology 19:369-383.
19. Hermann J, Pecka M, von Gersdorff H, Grothe B, Klug A (2007) Synaptic transmission at the calyx of Held under in vivo like activity levels. J Neurophysiol 98:807-820. (Pubitemid 47236034)
20. Hoffpauir BK, Grimes JL, Mathers PH, Spirou GA (2006) Synaptogenesis of the calyx of Held: rapid onset of function and one-to-one morphological innervation. J Neurosci 26:5511-5523.
21. Huangfu M, Saunders JC (1983) Auditory development in the mouse: structural maturation of the middle ear. J Morphol 176:249-259.
22. Ison JR, Allen PD, O'Neill WE (2007) Age-related hearing loss in C57BL/6J mice has both frequency-specific and non-frequency-specific components that produce a hyperacusis-like exaggeration of the acoustic startle reflex. J Assoc Res Otolaryngol 8:539-550.
23. Iwasaki S, Takahashi T (1998) Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J Physiol 509:419-423. (Pubitemid 28287000)
24. Iwasaki S, Takahashi T (2001) Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol 534:861-871. (Pubitemid 32700882)
25. Jones TA, Jones SM (2000) Spontaneous activity in the statoacoustic ganglion of the chicken embryo. J Neurophysiol 83:1452-1468. (Pubitemid 30159573)
26. Jones TA, Jones SM, Paggett KC (2001) Primordial rhythmic bursting in embryonic cochlear ganglion cells. J Neurosci 21:8129-8135.
27. Jones TA, Leake PA, Snyder RL, Stakhovskaya O, Bonham B (2007) Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats. J Neurophysiol 98:1898-1908. (Pubitemid 47584380)
28. Joshi I, Wang LY (2002) Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem. J Physiol 540:861-873. (Pubitemid 35190159)
29. Kaltenbach JA, Falzarano PR (1994) Postnatal development of the hamster cochlea. I. Growth of hair cells and the organ of Corti. J Comp Neurol 340:87-97. (Pubitemid 24036460)
30. Kamiya K, Takahashi K, Kitamura K, Momoi T, Yoshikawa Y (2001) Mitosis and apoptosis in postnatal auditory system of the C3H/He strain. Brain Res 901:296-302. (Pubitemid 32718835)
31. Kandler K, Friauf E (1993) Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328:161-184. (Pubitemid 23057958)
32. Kil J, Kageyama GH, Semple MN, KitzesLM (1995) Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil. J Comp Neurol 353:317-340.
33. Kitzes LM, Kageyama GH, Semple MN, Kil J (1995) Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J Comp Neurol 353:341-363.
34. Kopp-Scheinpflug C, Fuchs K, Lippe WR, Tempel BL, Rübsamen R (2003a) Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J Neurosci 23:9199-9207. (Pubitemid 37243821)
35. Kopp-Scheinpflug C, Lippe WR, Dörrscheidt GJ, Rübsamen R (2003b) The medial nucleus of the trapezoid body in the gerbil is more than a relay: comparison of pre- and postsynaptic activity. J Assoc Res Otolaryngol 4:1-23.
36. Kopp-Scheinpflug C, Tolnai S, Malmierca MS, Rübsamen R (2008) The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154:160-170.
37. Kros CJ (2007) How to build an inner hair cell: challenges for regeneration. Hear Res 227:3-10.
38. Kros CJ, Ruppersberg JP, Rüsch A (1998) Expression of a potassium current in inner hair cells during development of hearing in mice. Nature 394:281-284.
39. Leake PA, Hradek GT, Chair L, Snyder RL (2006) Neonatal deafness results in degraded topographic specificity of auditory nerve projections to the cochlear nucleus in cats. J Comp Neurol 497:13-31. (Pubitemid 43844565)
40. + channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J Neurosci 25:3724-3738.
41. Leao RN, Sun H, Svahn K, Berntson A, Youssoufian M, Paolini AG, Fyffe RE, Walmsley B (2006) Topographic organization in the auditory brainstem of juvenile mice is disrupted in congenital deafness. J Physiol 571:563-578. (Pubitemid 43329547)
42. Li HS, Borg E (1991) Age-related loss of auditory sensitivity in two mouse genotypes. Acta Otolaryngol 111:827-834.
43. Lippe WR (1994) Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14:1486-1495.
44. Marcotti W, Johnson SL, Holley MC, Kros CJ (2003) Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. J Physiol 548:383-400. (Pubitemid 36527462)
45. McKay SM, Oleskevich S (2007) The role of spontaneous activity in development of the endbulb of Held synapse. Hear Res 230:53-63.
46. Mc Laughlin M, van der Heijden M, Joris PX (2008) How secure is in vivo synaptic transmission at the calyx of Held? J Neurosci 28:10206-10219.
47. MikaelianDO (1979) Development and degeneration of hearing in the C57/ b16 mouse: relation of electrophysiologic responses from the round window and cochlear nucleus to cochlear anatomy and behavioral responses. Laryngoscope 89:1-15.
48. MorestDK (1968) The growth of synaptic endings in the mammalian brain: a study of the calyces of the trapezoid body. Z Anat Entwicklungsgesch 127:201-220.
49. Müller M, von Hünerbein K, Hoidis S, Smolders JW (2005) A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202:63-73. (Pubitemid 40469771)
50. Overstreet EH 3rd, Temchin AN, Ruggero MA (2002) Passive basilar membrane vibrations in gerbil neonates: mechanical bases of cochlear maturation. J Physiol 545:279-288.
51. Paolini AG, FitzGerald JV, Burkitt AN, ClarkGM (2001) Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat. Hear Res 159:101-116.
52. Rubel EW (1978) Ontogeny of structure and function in the vertebrate auditory system. In: Handbook of sensory physiology, Vol 9. Development of sensory systems (Jacobson M, ed), pp 213-229. Berlin: Springer.
53. Rubel EW, Lippe WR, RyalsBM (1984) Development of the place principle. Ann Otol Rhinol Laryngol 93:609-615.
54. Rübsamen R, Schäfer M (1990) Ontogenesis of auditory fovea representation in the inferior colliculus of the Sri Lankan rufous horseshoe bat, Rhinolophus rouxi. J Comp Physiol A 167:757-769.
55. Schneggenburger R, Forsythe ID (2006) The calyx of Held. Cell Tissue Res 326:311-337.
56. Shnerson A, Willott JF (1979) Development of inferior colliculus response properties in C57BL/6J mouse pups. Exp Brain Res 37:373-385. (Pubitemid 10225809)
57. Smith PH, Rhode WS (1987) Characterization of HRP-labeled globular bushy cells in the cat anteroventral cochlear nucleus. J Comp Neurol 266:360-375.
58. Smith PH, Joris PX, Carney LH, Yin TC (1991) Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304:387-407.
59. Smith PH, Joris PX, Yin TC (1998) Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. J Neurophysiol 79:3127-3142.
60. Sommer I, Lingenhöhl K, Friauf E (1993) Principal cells of the rat medial nucleus of the trapezoid body: an intracellular in vivo study of their physiology and morphology. Exp Brain Res 95:223-239. (Pubitemid 23288332)
61. Spirou GA, Brownell WE, ZidanicM (1990) Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J Neurophysiol 63:1169-1190.
62. Taberner AM, Liberman MC (2005) Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93:557-569.
63. Taschenberger H, von Gersdorff H (2000) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173. (Pubitemid 32042919)
64. Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127-143.
65. Tollin DJ, Yin TC (2005) Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25:10648-10657.
66. Tolnai S, Englitz B, Kopp-Scheinpflug C, Dehmel S, Jost J, Rübsamen R (2008a) Dynamic coupling of excitatory and inhibitory responses in the medial nucleus of the trapezoid body. Eur J Neurosci 27:3191-3204. (Pubitemid 351847316)
67. Tolnai S, Hernandez O, Englitz B, Rübsamen R, MalmiercaMS (2008b) The medial nucleus of the trapezoid body in rat: spectral and temporal properties vary with anatomical location of the units. Eur J Neurosci 27:2587-2598.
68. Tritsch NX, Bergles DE (2009) Inner hair cell calcium action potentials pattern neural activity before the onset of hearing. Assoc Res Otolaryngol Abstr 32:774.
69. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450:50-55. (Pubitemid 350070568)
70. von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53-64.
71. Walsh BT, Miller JB, Gacek RR, Kiang NYS (1972) Spontaneous activity in the eighth cranial nerve of the cat. Int J Neurosci 3:221-236.
72. Walsh EJ, McGee J (1987) Postnatal development of auditory nerve and cochlear nucleus neuronal responses in kittens. Hear Res 28:97-116.
73. Walsh EJ, McGee J (1988) Rhythmic discharge properties of caudal cochlear nucleus neurons during postnatal development in cats. Hear Res 36:233-247.
74. Woolf NK, Ryan AF (1988) Contributions of the middle ear to the development of function in the cochlea. Hear Res 35:131-142. (Pubitemid 18236219)
75. Yin TC (2002) Neuronal mechanisms of encoding binaural localization cues in auditory brainstem. In: Integrative functions in the mammalian auditory pathway (Oertel D, Popper AN, Fay RR, eds), pp 99-159. New York: Springer.
76. Young ED, Robert JM, ShofnerWP (1988) Regularity and latency of units in ventral cochlear nucleus: implications for unit classification and generation of response properties. J Neurophysiol 60:1-29.