Chemical synaptic transmission onto superficial stellate cells of the mouse dorsal cochlear nucleus

Journal of Neurophysiology

Volumn 111, Issue 9, 2014, Pages 1812-1822

  Apostolides, Pierre F ^a   Trussell, Laurence O ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Auditory; Cochlear nucleus; Inhibition; Interneuron

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; AMPA RECEPTOR; GLYCINE RECEPTOR; GLYCINE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CEREBELLUM; DORSAL COCHLEAR NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIAL; EXOCYTOSIS; GABAERGIC TRANSMISSION; INTERNEURON; MOUSE; NERVE ENDING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; SPINDLE CELL; STELLATE CELL; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; COCHLEAR NUCLEUS; CYTOLOGY; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPSE;

ANIMALS; COCHLEAR NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIALS; MICE; MICE, INBRED C57BL; NEURONS; RECEPTORS, AMPA; RECEPTORS, GABA-A; RECEPTORS, GLYCINE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 84900828833     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00821.2013     Document Type: Article

References (58)

1. Apostolides PF, Trussell LO. Rapid activity-independent turnover of vesicular transmitter content at a mixed glycine/GABA synapse. J Neurosci 33: 4768-4781, 2013a.
2. Apostolides PF, Trussell LO. Regulation of interneuron excitability by gap junction coupling with principal cells. Nat Neurosci 16: 1764-1772, 2013b.
3. Arenkiel BR, Peca J, Davison IG, Feliciano C, Deisseroth K, Augustine GJ, Ehlers MD, Feng G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron 54: 205-218, 2007.
4. Barmack NH, Yakhnitsa V. Functions of interneurons in mouse cerebellum. J Neurosci 28: 1140-1152, 2008.
5. Bell CC, Han V, Sawtell NB. Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31: 1-24, 2008.
6. 2+]i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15: 2777-2787, 1995.
7. Carter AG, Regehr WG. Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20: 4423-4434, 2000.
8. Carter AG, Regehr WG. Quantal events shape cerebellar interneuron firing. Nat Neurosci 5: 1309-1318, 2002.
9. Clark BA, Cull-Candy SG. Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22: 4428-4436, 2002.
10. Coddington LT, Rudolph S, Vande Lune P, Overstreet-Wadiche L, Wadiche JI. Spillover-mediated feedforward inhibition functionally segregates interneuron activity. Neuron 78: 1050-1062, 2013.
11. Crowley JJ, Carter AG, Regehr WG. Fast vesicle replenishment and rapid recovery from desensitization at a single synaptic release site. J Neurosci 27: 5448-5460, 2007.
12. Davis KA, Miller RL, Young ED. Effects of somatosensory and parallel-fiber stimulation on neurons in dorsal cochlear nucleus. J Neurophysiol 76: 3012-3024, 1996.
13. Davis KA, Young ED. Granule cell activation of complex-spiking neurons in dorsal cochlear nucleus. J Neurosci 17: 6798-6806, 1997.
14. Davis KA, Young ED. Pharmacological evidence of inhibitory and disinhibitory neuronal circuits in dorsal cochlear nucleus. J Neurophysiol 83: 926-940, 2000.
15. Doiron B, Zhao Y, Tzounopoulos T. Combined LTP and LTD of modulatory inputs controls neuronal processing of primary sensory inputs. J Neurosci 31: 10579-10592, 2011.
16. Gardner SM, Trussell LO, Oertel D. Time course and permeation of synaptic AMPA receptors in cochlear nuclear neurons correlate with input. J Neurosci 19: 8721-8729, 1999.
17. 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.
18. Glitsch M, Marty A. Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19: 511-519, 1999.
19. Golding NL, Oertel D. Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. J Neurophysiol 78: 248-260, 1997.
20. Gomeza J, Ohno K, Hülsmann S, Armsen W, Eulenburg V, Richter DW, Laube B, Betz H. Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 40: 797-806, 2003.
21. Hägglund M, Borgius L, Dougherty KJ, Kiehn O. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat Neurosci 13: 246-252, 2010.
22. Hughes DI, Mackie M, Nagy GG, Riddell JS, Maxwell DJ, Szabó G, Erdélyi F, Veress G, Szucs P, Antal M, Todd AJ. P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase- 65 and originate from cells in deep medial dorsal horn. Proc Natl Acad Sci USA 102: 9038-9043, 2005.
23. Isaac JTR, Ashby MC, McBain CJ. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54: 859-871, 2007.
24. Isope P, Franconville R, Barbour B, Ascher P. Repetitive firing of rat cerebellar parallel fibres after a single stimulation. J Physiol 554: 829-839, 2004.
25. Jackson AC, Nicoll RA. Stargazin (TARP gamma-2) is required for compartment- specific AMPA receptor trafficking and synaptic plasticity in cerebellar stellate cells. J Neurosci 31: 3939-3952, 2011.
26. Kamboj SK, Swanson GT, Cull-Candy SG. Intracellular spermine confers rectification on rat calcium-permeable AMPA and kainate receptors. J Physiol 486: 297-303, 1995.
27. Kanold PO, Young ED. Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J Neurosci 21: 7848-7858, 2001.
28. Kondo S, Marty A. Synaptic currents at individual connections among stellate cells in rat cerebellar slices. J Physiol 509: 221-232, 1998.
29. Kuo SP, Trussell LO. Spontaneous spiking and synaptic depression underlie noradrenergic control of feed-forward inhibition. Neuron 171: 306-318, 2011.
30. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA, Kullmann DM. Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315: 1262-1266, 2007.
31. Liu SQ, Cull-Candy SG. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405: 454-458, 2000.
32. Mancilla JG, Manis PB. Two distinct types of inhibition mediated by cartwheel cells in the dorsal cochlear nucleus. J Neurophysiol 102: 1287-1295, 2009.
33. Manis PB. Responses to parallel fiber stimulation in the guinea pig dorsal cochlear nucleus in vitro. J Neurophysiol 61: 149-161, 1989.
34. Manis PB, Spirou GA, Wright DD, Paydar S, Ryugo DK. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J Comp Neurol 348: 261-276, 1994.
35. May BJ. Role of the dorsal cochlear nucleus in the sound localization behavior of cats. Hear Res 148: 74-87, 2000.
36. Middleton JW, Kiritani T, Pedersen C, Turner JG, Shepherd GMG, Tzounopoulos T. Mice with behavioral evidence of tinnitus exhibit dorsal cochlear nucleus hyperactivity because of decreased GABAergic inhibition. Proc Natl Acad Sci USA 108: 7601-7606, 2011.
37. Mugnaini E. GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: light and electron microscopic immunocytochemistry. J Comp Neurol 235: 61-81, 1985.
38. Nahir B, Jahr CE. Activation of extrasynaptic NMDARs at individual parallel fiber-molecular layer interneuron synapses in cerebellum. J Neurosci 33: 16323-16333, 2013.
39. Oertel D, Wright S, Cao XJ, Ferragamo M, Bal R. The multiple functions of T stellate/multipolar/chopper cells in the ventral cochlear nucleus. Hear Res 276: 61-69, 2011.
40. Oertel D, Young ED. What's a cerebellar circuit doing in the auditory system? Trends Neurosci 27: 104-110, 2004.
41. Oldfield CS, Marty A, Stell BM. Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states. Proc Natl Acad Sci USA 107: 13153-13158, 2010.
42. Osen KK, Mugnaini E. Neuronal circuits in the dorsal cochlear nucleus. In: Neuronal Mechanisms of Hearing, edited by Syka J and Aitkin L. New York: Plenum, 1981, p. 119-133.
43. Palay SL, Chan-Palay V. Cerebellar Cortex: Cytology and Organization. New York: Springer, 1974.
44. Pouzat C, Marty A. Autaptic inhibitory currents recorded from interneurones in rat cerebellar slices. J Physiol 509: 777-783, 1998.
45. Requarth T, Sawtell NB. Neural mechanisms for filtering self-generated sensory signals in cerebellum-like circuits. Curr Opin Neurobiol 21: 602-608, 2011.
46. Roberts MT, Bender KJ, Trussell LO. Fidelity of complex spike-mediated synaptic transmission between inhibitory interneurons. J Neurosci 28: 9440-9450, 2008.
47. Roberts MT, Trussell LO. Molecular layer inhibitory interneurons provide feedforward and lateral inhibition in the dorsal cochlear nucleus. J Neurophysiol 104: 2462-2473, 2010.
48. Rousseau F, Aubrey KR, Supplisson S. The glycine transporter GlyT2 controls the dynamics of synaptic vesicle refilling in inhibitory spinal cord neurons. J Neurosci 28: 9755-9768, 2008.
49. Rozov A, Burnashev N. Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression. Nature 401: 594-598, 1999.
50. Rubio ME, Juiz JM. Differential distribution of synaptic endings containing glutamate, glycine, and GABA in the rat dorsal cochlear nucleus. J Comp Neurol 477: 253-272, 2004.
51. Soto D, Coombs ID, Kelly L, Farrant M, Cull-Candy SG. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat Neurosci 10: 1260-1267, 2007.
52. Sutherland DP, Masterton RB, Glendenning KK. Role of acoustic striae in hearing: Reflexive responses to elevated sound sources. Behav Brain Res 97: 1-12, 1998.
53. Tzounopoulos T, Kim Y, Oertel D, Trussell LO. Cell-specific, spike timingdependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7: 719-725, 2004.
54. Tzounopoulos T, Rubio ME, Keen JE, Trussell LO. Coactivation of preand postsynaptic signaling mechanisms determines cell-specific spike-timing- dependent plasticity. Neuron 54: 291-301, 2007.
55. Vincent P, Marty A. Fluctuations of inhibitory postsynaptic currents in Purkinje cells from rat cerebellar slices. J Physiol 494: 183-199, 1996.
56. Wouterlood FG, Mugnaini E, Osen KK, Dahl AL. Stellate neurons in rat dorsal cochlear nucleus studies with combined Golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions. J Neurocytol 13: 639-664, 1984.
57. Zeilhofer HU, Studler B, Arabadzisz D, Schweizer C, Ahmadi S, Layh B, Bösl MR, Fritschy JM. Glycinergic neurons expressing enhanced green fluorescent protein in bacterial artificial chromosome transgenic mice. J Comp Neurol 482: 123-141, 2005.
58. Zhang S, Oertel D. Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J Neurophysiol 69: 1384-1397, 1993.