Context-dependent effects of NMDA receptors on precise timing information at the endbulb of held in the cochlear nucleus

Journal of Neurophysiology

Volumn 102, Issue 5, 2009, Pages 2627-2637

  Pliss, Lioudmila ^a   Yang, Hua ^a   Xu Friedman, Matthew A ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACOUSTIC NERVE FIBER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; COCHLEAR NUCLEUS; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; LATENT PERIOD; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOUND DETECTION; SYNAPTIC MEMBRANE; VOLTAGE CLAMP;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICAL PHENOMENA; BIOPHYSICS; COCHLEAR NERVE; COCHLEAR NUCLEUS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; MICE; MICE, INBRED CBA; NEURAL CONDUCTION; NEURONS; PATCH-CLAMP TECHNIQUES; PIPERAZINES; PROBABILITY; QUINOXALINES; REACTION TIME; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; TIME PERCEPTION;

EID: 70449394564     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00111.2009     Document Type: Article

References (62)

1. Augustinaite S, Heggelund P. Changes in firing pattern of lateral geniculate neurons caused by membrane potential dependent modulation of retinal input through NMDA receptors. J Physiol 582: 297-315, 2007. (Pubitemid 46993576)
2. Bellingham MC, Lim R, Walmsley B. Developmental changes in EPSC quantal size and quantal content at a central glutamatergic synapse in rat. J Physiol 511: 861-869, 1998. (Pubitemid 28456913)
3. Blitz DM, Regehr WG. Retinogeniculate synaptic properties controlling spike number and timing in relay neurons. J Neurophysiol 90: 2438-2450, 2003.
4. Brawer JR, Morest DK. Relations between auditory nerve endings and cell types in the cat's anteroventral cochlear nucleus seen with the Golgi method and Nomarski optics. J Comp Neurol 160: 491-506, 1975.
5. Carr CE. Processing of temporal information in the brain. Annu Rev Neurosci 16: 223-243, 1993.
6. Carr CE, Friedman MA. Evolution of time coding systems. Neural Comput 11: 1-20, 1999.
7. Dan Y, Alonso JM, Usrey WM, Reid RC. Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat Neurosci 1: 501-507, 1998. (Pubitemid 128406061)
8. Ehret G. Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1: 179-184, 1976.
9. Ferragamo MJ, Oertel D. Functional circuitry of the cochlear nucleus: in vitro studies in slices. In: Handbook of Mouse Auditory Research: From Behavior to Molecular Biology, edited by Willott JF. Boca Raton, FL: CRC, 2001, p. 297-315.
10. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, Monyer H. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17: 2469-2476, 1997. (Pubitemid 27137413)
11. Friedland DR, Eernisse R, Popper P. Potassium channel gene expression in the rat cochlear nucleus. Hear Res 228: 31-43, 2007. (Pubitemid 46660399)
12. Futai K, Okada M, Matsuyama K, Takahashi T. High-fidelity transmission acquired via a developmental decrease in NMDA receptor expression at an auditory synapse. J Neurosci 21: 3342-3349, 2001. (Pubitemid 32422799)
13. Gardner SM, Trussell LO, Oertel D. Correlation of AMPA receptor subunit composition with synaptic input in the mammalian cochlear nuclei. J Neurosci 21: 7428-7437, 2001. (Pubitemid 32846990)
14. Hahnloser RH, Kozhevnikov AA, Fee MS. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419: 65-70, 2002.
15. Harris EW, Ganong AH, Monaghan DT, Watkins JC, Cotman CW. Action of 3-((+/-)-2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP): a new and highly potent antagonist of N-methyl-D-aspartate receptors in the hippocampus. Brain Res 382: 174-177, 1986.
16. Harsch A, Robinson HP. Postsynaptic variability of firing in rat cortical neurons: the roles of input synchronization and synaptic NMDA receptor conductance. J Neurosci 20: 6181-6192, 2000. (Pubitemid 30658412)
17. Heiligenberg . Neural Nets in Electric Fish. Cambridge, MA: Bradford Book, 1991.
18. Hopkins CD, Bass AH. Temporal coding of species recognition signals in an electric fish. Science 212: 85-87, 1981.
19. Isaacson JS, Walmsley B. Counting quanta: direct measurements of transmitter release at a central synapse. Neuron 15: 875-884, 1995a.
20. Isaacson JS, Walmsley B. Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus. J Neurophysiol 73: 964-973, 1995b.
21. Isaacson JS, Walmsley B. Amplitude and time course of spontaneous and evoked excitatory postsynaptic currents in bushy cells of the anteroventral cochlear nucleus. J Neurophysiol 76: 1566-1571, 1996. (Pubitemid 26322603)
22. Joelson D, Schwartz IR. Development of N-methyl-D-aspartate receptor subunit immunoreactivity in the neonatal gerbil cochlear nucleus. Microsc Res Tech 41: 246-262, 1998. (Pubitemid 28208631)
23. Johnson DH. The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J Acoust Soc Am 68: 1115-1122, 1980.
24. Joris PX, Smith PH, Yin TC. Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J Neurophysiol 71: 1037-1051, 1994. (Pubitemid 24094873)
25. Joshi I, Wang LY. Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brain stem. J Physiol 540: 861-873, 2002. (Pubitemid 35190159)
26. Kamiya K, Takahashi K, Kitamura K, Momoi T, Yoshikawa Y. Mitosis and apoptosis in postnatal auditory system of the C3H/He strain. Brain Res 901: 296-302, 2001. (Pubitemid 32718835)
27. Kawasaki M, Guo YX. Neuronal circuitry for comparison of timing in the electrosensory lateral line lobe of the African wave-type electric fish Gymnarchus niloticus. J Neurosci 16: 380-391, 1996. (Pubitemid 26010724)
28. Kiang NY, Pfeiffer RR, Warr WB, Backus AS. Stimulus coding in the cochlear nucleus. Ann Otol Rhinol Laryngol 74: 463-485, 1965.
29. Klumpp RG, Eady HR. Some measurements of interaural time difference thresholds. J Acoust Soc Am 28: 859-860, 1956.
30. Koike-Tani M, Saitoh N, Takahashi T. Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci 25: 199-207, 2005. (Pubitemid 40110781)
31. Lehmann J, Schneider J, McPherson S, Murphy DE, Bernard P, Tsai C, Bennett DA, Pastor G, Steel DJ, Boehm C, Cheney DL, Liebman JM, Williams M, Woud PL. CPP, a selective N-methyl-D-aspartate (NMDA)- type receptor antagonist: characterization in vitro and in vivo. J Pharmacol Exp Ther 240: 737-746, 1987. (Pubitemid 17043569)
32. Limb CJ, Ryugo DK. Development of primary axosomatic endings in the anteroventral cochlear nucleus of mice. J Assoc Res Otolaryngol 1: 103-119, 2000.
33. Lorente de Nó R. The Primary Acoustic Nuclei. New York: Raven, 1981.
34. Louage DH, van der Heijden M, Joris PX. Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise. J Neurosci 25: 1560-1570, 2005.
35. Mainen ZF, Sejnowski TJ. Reliability of spike timing in neocortical neurons. Science 268: 1503-1506, 1995.
36. Manis PB, Marx SO. Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11: 2865-2880, 1991.
37. Miyata M, Imoto K. Different composition of glutamate receptors in corticothalamic and lemniscal synaptic responses and their roles in the firing responses of ventrobasal thalamic neurons in juvenile mice. J Physiol 575: 161-174, 2006. (Pubitemid 44178135)
38. Moiseff A, Konishi M. Neuronal and behavioral sensitivity to binaural time differences in the owl. J Neurosci 1: 40-48, 1981. (Pubitemid 11021313)
39. Oertel D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3: 2043-2053, 1983. (Pubitemid 14233765)
40. Oertel D. Use of brain slices in the study of the auditory system: spatial and temporal summation of synaptic inputs in cells in the anteroventral cochlear nucleus of the mouse. J Acoust Soc Am 78: 328-333, 1985. (Pubitemid 15064055)
41. Oleskevich S, Clements J, Walmsley B. Release probability modulates short-term plasticity at a rat giant terminal. J Physiol 524: 513-523, 2000. (Pubitemid 30229515)
42. Paolini AG, FitzGerald JV, Burkitt AN, Clark GM. Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat. Hear Res 159: 101-116, 2001.
43. Robinson HP, Kawai N. Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49: 157-165, 1993. (Pubitemid 23350479)
44. Romand R. The roles of retinoic acid during inner ear development. Curr Top Dev Biol 57: 261-291, 2003. (Pubitemid 137639491)
45. Rothman JS, Manis PB. The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J Neurophysiol 89: 3097-3113, 2003.
46. Rouiller EM, Ryugo DK. Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J Comp Neurol 225: 167-186, 1984.
47. Ryugo DK, Fekete DM. Morphology of primary axosomatic endings in the anteroventral cochlear nucleus of the cat: a study of the endbulbs of Held. J Comp Neurol 210: 239-257, 1982.
48. Ryugo DK, Montey KL, Wright AL, Bennett ML, Pongstaporn T. Postnatal development of a large auditory nerve terminal: the endbulb of Held in cats. Hear Res 216-217: 100-115, 2006. (Pubitemid 44172930)
49. Sachs MB, Abbas PJ. Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J Acoust Soc Am 56: 1835-1847, 1974.
50. Sato K, Kuriyama H, Altschuler RA. Differential distribution of NMDA receptor subunit mRNA in the rat cochlear nucleus. Microsc Res Tech 41: 217-223, 1998. (Pubitemid 28208628)
51. Sharp AA, O'Neil MB, Abbott LF, Marder E. The dynamic clamp: artificial conductances in biological neurons. Trends Neurosci 16: 389-394, 1993. (Pubitemid 23283398)
52. Taberner AM, Liberman MC. Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93: 557-569, 2005.
53. Taschenberger H, Leao RM, Rowland KC, Spirou GA, von Gersdorff H. Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36: 1127-1143, 2002. (Pubitemid 36044513)
54. Taschenberger H, von Gersdorff H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20: 9162-9173, 2000. (Pubitemid 32042919)
55. Wang Y, Manis PB. Synaptic transmission at the cochlear nucleus endbulb synapse during age-related hearing loss in mice. J Neurophysiol 94: 1814- 1824, 2005.
56. Wang Y, Manis PB. Short-term synaptic depression and recovery at the mature mammalian endbulb of Held synapse in mice. J Neurophysiol 100: 1255-1264, 2008.
57. Wu SH, Ma CL, Kelly JB. Contribution of AMPA, NMDA, and GABA(A) receptors to temporal pattern of postsynaptic responses in the inferior colliculus of the rat. J Neurosci 24: 4625-4634, 2004.
58. Xu-Friedman MA, Regehr WG. Dynamic-clamp analysis of the effects of convergence on spike timing. I. Many synaptic inputs. J Neurophysiol 94: 2512-2525, 2005a. (Pubitemid 41324675)
59. Xu-Friedman MA, Regehr WG. Dynamic-clamp analysis of the effects of convergence on spike timing. II. Few synaptic inputs. J Neurophysiol 94: 2526-2534, 2005b. (Pubitemid 41324676)
60. Yang H, Xu-Friedman MA. Relative roles of different mechanisms of depression at the mouse endbulb of held. J Neurophysiol 99: 2510-2521, 2008.
61. Youssoufian M, Oleskevich S, Walmsley B. Development of a robust central auditory synapse in congenital deafness. J Neurophysiol 94: 3168-3180, 2005. (Pubitemid 41504759)
62. Yu AC, Margoliash D. Temporal hierarchical control of singing in birds. Science 273: 1871-1875, 1996.