Short-term synaptic depression and recovery at the mature mammalian endbulb of Held synapse in mice

Journal of Neurophysiology

Volumn 100, Issue 3, 2008, Pages 1255-1264

  Wang, Yong ^a,b   Manis, Paul B ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALMIDAZOLIUM;

ACOUSTIC NERVE FIBER; ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CALCIUM CELL LEVEL; COCHLEAR NERVE; COCHLEAR NUCLEUS; CONTROLLED STUDY; IMMATURITY; IN VIVO STUDY; MOUSE; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; SHORT TERM SYNAPTIC DEPRESSION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCIUM; COCHLEAR NUCLEUS; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; ENZYME INHIBITORS; EVOKED POTENTIALS, AUDITORY; EXCITATORY POSTSYNAPTIC POTENTIALS; IMIDAZOLES; MICE; MICE, INBRED CBA; NEURAL INHIBITION; NEURONAL PLASTICITY; OLIGOPEPTIDES; PRESYNAPTIC TERMINALS; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 57349103102     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.90715.2008     Document Type: Article

References (66)

1. 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.
2. Bellingham MC, Walmsley B. A novel presynaptic inhibitory mechanism underlies paired pulse depression at a fast central synapse. Neuron 23: 159-170, 1999.
3. 2+ signal. Nat Neurosci 8: 426-434, 2005.
4. Bollmann JH, Sakmann B, Borst JG. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289: 953-957, 2000.
5. Brenowitz S, Trussell LO. Maturation of synaptic transmission at end-bulb synapses of the cochlear nucleus. J Neurosci 21: 9487-9498, 2001a.
6. Brenowitz S, Trussell LO. Minimizing synaptic depression by control of release probability. J Neurosci 21: 1857-1867, 2001b.
7. Caspary DM, Backoff PM, Finlayson PG, Palombi PS. Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J Neurophysiol 72: 2124-2133, 1994.
8. Dittman JS, Regehr WG. Contributions of calcium-dependent and calciumin-dependent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci 16: 1623-1633, 1996.
9. Dittman JS, Regehr WG. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18: 6147-6162, 1998.
10. Fedchyshyn MJ, Wang LY. Developmental transformation of the release modality at the calyx of held synapse. J Neurosci 25: 4131-4140, 2005.
11. 2+-binding proteins calretinin and parvalbumin at the calyx of held of rats and mice. Eur J Neurosci 20: 1473-1482, 2004.
12. Forsythe ID, Tsujimoto T, Barnes-Davies M, Cuttle MF, Takahashi T. Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20: 797-807, 1998.
13. Helmchen F, Borst JG, Sakmann B. Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72: 1458-1471, 1997.
14. Hermann J, Pecka M, von Gersdorff H, Grothe B, Klug A. Synaptic transmission at the calyx of Held under in vivo like activity levels. J Neurophysiol 98: 807-820, 2007.
15. 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.
16. 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.
17. Kachar B. Asymmetric illumination contrast: a method of image formation for video light microscopy. Science 227: 766-768, 1985.
18. Kindmark H, Kohler M, Gerwins P, Larsson O, Khan A, Wahl MA, Berggren PO. The imidazoline derivative calmidazolium inhibits voltage-gated Ca(2+)-channels and insulin release but has no effect on the phospholipase C system in insulin producing RINm5F-cells. Biosci Rep 14: 145-158, 1994.
19. Kopp-Scheinpflug C, Dehmel S, Dorrscheidt GJ, Rubsamen R. Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. J Neurosci 22: 11004-11018, 2002.
20. Kopp-Scheinpflug C, Fuchs K, Lippe WR, Tempel BL, Rubsamen R. Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J Neurosci 23: 9199-9207, 2003.
21. + channels: locus, development, and recovery from inactivation at a high-fidelity synapse. J Neurosci 25: 3724-3738, 2005.
22. Li J, Young ED. Discharge-rate dependence of refractory behavior of cat auditory-nerve fibers. Hear Res 69: 151-162, 1993.
23. Liberman MC. Auditory-nerve response from cats raised in a low-noise chamber. J Acoust Soc Am 63: 442-455, 1978.
24. Liberman MC. Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J Comp Neurol 313: 240-258, 1991.
25. Lu T, Trussell LO. Development and elimination of endbulb synapses in the chick cochlear nucleus. J Neurosci 27: 808-817, 2007.
26. Manis PB. Biophysical specialization of neurons that encode timing. In: The Senses, A Comphensive Reference, edited by Basbaum AI, Kaneko A, Shepherd GM, Wesseling JF. San Diego, CA: Academic, 2008, p. 565-586.
27. 2+ channels in smooth muscle from rat vas deferens. Br J Pharmacol 109: 137-141, 1993.
28. Nicol MJ, Walmsley B. Ultrastructural basis of synaptic transmission between endbulbs of Held and bushy cells in the rat cochlear nucleus. J Physiol 539: 713-723, 2002.
29. Ohlemiller KK, Echteler SM, Siegel JH. Factors that influence rate-versus-intensity relations in single cochlear nerve fibers of the gerbil. J Acoust Soc Am 90: 274-287, 1991.
30. Oleskevich S, Clements J, Walmsley B. Release probability modulates short-term plasticity at a rat giant terminal. J Physiol 524: 513-523, 2000.
31. Oleskevich S, Walmsley B. Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. J Physiol 540: 447-455, 2002.
32. Oleskevich S, Youssoufian M, Walmsley B. Presynaptic plasticity at two giant auditory synapses in normal and deaf mice. J Physiol 560: 709-719, 2004.
33. Otis T, Zhang S, Trussell LO. Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16: 7496-7504, 1996.
34. Pfeiffer RR. Anteroventral cochlear nucleus: wave forms of extracellularly recorded spike potentials. Science 154: 667-668, 1966.
35. Raman IM, Trussell LO. The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9: 173-186, 1992.
36. Renden R, Taschenberger H, Puente N, Rusakov DA, Duvoisin R, Wang LY, Lehre KP, von Gersdorff H. Glutamate transporter studies reveal the pruning of metabotropic glutamate receptors and absence of AMPA receptor desensitization at mature calyx of held synapses. J Neurosci 25: 8482-8497, 2005.
37. Rodieck RW, Kiang NY, Gerstein GL. Some quantitative methods for the study of spontaneous activity of single neurons. Biophys J 2: 351-368, 1962.
38. Rothman JS, Young ED, Manis PB. Convergence of auditory nerve fibers onto bushy cells in the ventral cochlear nucleus: implications of a computational model. J Neurophysiol 70: 2562-2583, 1993.
39. Ryugo DK, Parks TN. Primary innervation of the avian and mammalian cochlear nucleus. Brain Res Bull 60: 435-456, 2003.
40. Sachs MB, Abbas PJ. Rate versus level functions for auditory-nerve fibers in cats: tone-burst stimuli. J Acoust Soc America 56: 1835-1847, 1974.
41. Sakaba T, Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131, 2001a.
42. Sakaba T, Neher E. Preferential potentiation of fast-releasing synaptic vesicles by cAMP at the calyx of Held. Proc Natl Acad Sci USA 98: 331-336, 2001b.
43. Sakaba T, Neher E. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424: 775-778, 2003.
44. Schneggenburger R, Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406: 889-893, 2000.
45. Spirou GA, Chirila FV, von Gersdorff H, Manis PB. Heterogeneous Ca(2+) influx along the adult calyx of held: a structural and computational study. Neuroscience 154: 171-185, 2008.
46. Stevens CF, Wesseling JF. Identification of a novel process limiting the rate of synaptic vesicle cycling at hippocampal synapses. Neuron 24: 1017-1028, 1999.
47. Taberner AM, Liberman MC. Response properties of single auditory nerve fibers in the mouse. J Neurophysiol 93: 557-569, 2005.
48. Trussell LO. Central synapses that preserve auditory timing. In: The Senses: A Comprehensive Reference, edited by Basbaum AI, Kaneko A, Shepherd GM, Westheimer G. San Diego, CA: Academic, 2008, p. 587-602.
49. Trussell LO, Zhang S, Raman IM. Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10: 1185-1196, 1993.
50. Turecek R, Trussell LO. Presynaptic glycine receptors enhance transmitter release at a mammalian central synapse. Nature 411: 587-590, 2001.
51. von Gersdorff H, Borst JG. Short-term plasticity at the calyx of held. Nat Rev Neurosci 3: 53-64, 2002.
52. Wadel K, Neher E, Sakaba T. The coupling between synaptic vesicles and Ca(2+) channels determines fast neurotransmitter release. Neuron 53: 563-575, 2007.
53. Wang LY, Kaczmarek LK. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384-388, 1998.
54. 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.
55. Wang Y, Manis PB. Temporal coding by cochlear nucleus bushy cells in DBA/2J mice with early onset hearing loss. J Assoc Res Otolaryngol 7: 412-424, 2006.
56. Wickesberg RE, Oertel D. Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice. J Comp Neurol 268: 389-399, 1988.
57. Winter IM, Robertson D, Yates GK. Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibers. Hear Res 45: 191-202, 1990.
58. Wolfel M, Lou X, Schneggenburger R. A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J Neurosci 27: 3198-3210, 2007.
59. Wong AY, Graham BP, Billups B, Forsythe ID. Distinguishing between presynaptic and postsynaptic mechanisms of short-term depression during action potential trains. J Neurosci 23: 4868-4877, 2003.
60. Wu LG, Borst JG. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23: 821-832, 1999.
61. Xu J, Wu LG. The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46: 633-645, 2005.
62. 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.
63. 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.
64. Yang H, Xu-Friedman MA. Relative roles of different mechanisms of depression at the mouse endbulb of Held. J Neurophysiol 99: 2510-2521, 2008.
65. Zhang S, Trussell LO. A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705-718, 1994.
66. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.