Zones of enhanced glutamate release from climbing fibers in the mammalian cerebellum

Journal of Neuroscience

Volumn 30, Issue 21, 2010, Pages 7290-7299

  Paukert, Martin ^a   Huang, Yanhua H ^a,c   Tanaka, Kohichi ^b   Rothstein, Jeffrey D ^a   Bergles, Dwight E ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 4; GLUTAMIC ACID;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL VACUOLE; CLIMBING FIBER; CONTROLLED STUDY; IMMUNOREACTIVITY; INNERVATION; KNOCKOUT MOUSE; MAMMAL; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PURKINJE CELL; SPIKE; SPIKELET; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ASPARTIC ACID; CEREBELLUM; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY AMINO ACID TRANSPORTER 4; GABA ANTAGONISTS; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE FIBERS; NERVE TISSUE PROTEINS; PURKINJE CELLS; PYRIDAZINES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; ZINC;

EID: 77953048306     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5118-09.2010     Document Type: Article

References (63)

1. Alvina K, Walter JT, Kohn A, Ellis-Davies G, Khodakhah K (2008) Questioning the role of rebound firing in the cerebellum. Nat Neurosci 11:1256-1258.
2. Auger C, AttwellD(2000) Fast removal of synaptic glutamate by postsynaptic transporters. Neuron 28:547-558.
3. Bergles DE, Dzubay JA, Jahr CE (1997) Glutamate transporter currents in Bergmann glial cells follow the time course of extrasynaptic glutamate. Proc Natl Acad Sci U S A 94:14821-14825.
4. Blenkinsop TA, Lang EJ (2006) Block of inferior olive gap junctional coupling decreases Purkinje cell complex spike synchrony and rhythmicity. J Neurosci 26:1739-1748.
5. Brasnjo G, Otis TS (2001) Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron 31:607-616.
6. Brasnjo G, Otis TS (2004) Isolation of glutamate transport-coupled charge flux and estimation of glutamate uptake at the climbing fiber-Purkinje cell synapse. Proc Natl Acad Sci U S A 101:6273-6278.
7. Brenowitz SD, RegehrWG (2005) Associative short-term synaptic plasticity mediated by endocannabinoids. Neuron 45:419-431.
8. Brochu G, Maler L, Hawkes R (1990) Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol 291:538-552.
9. Carey MR, Regehr WG (2009) Noradrenergic control of associative synaptic plasticity by selective modulation of instructive signals. Neuron 62:112-122.
10. Clark BA, Barbour B (1997) Currents evoked in Bergmann glial cells by parallel fibre stimulation in rat cerebellar slices. J Physiol 502:335-350.
11. Clements JD, Silver RA (2000) Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci 23:105-113.
12. Coesmans M, Weber JT, De Zeeuw CI, Hansel C (2004) Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron 44:691-700.
13. Davie JT, Clark BA, Häusser M (2008) The origin of the complex spike in cerebellar Purkinje cells. J Neurosci 28:7599-7609.
14. Dehnes Y, Chaudhry FA, Ullensvang K, Lehre KP, Storm-Mathisen J, Danbolt NC (1998) The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci 18:3606-3619.
15. Dzubay JA, Otis TS (2002) Climbing fiber activation of metabotropic glutamate receptors on cerebellar Purkinje neurons. Neuron 36:1159-1167.
16. Eccles JC, Llinas R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol 182:268-296.
17. Foster KA, Regehr WG (2004) Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse. Neuron 43:119-131.
18. Foster KA, Kreitzer AC, Regehr WG (2002) Interaction of postsynaptic receptor saturation with presynaptic mechanisms produce a reliable synapse. Neuron 36:1115-1126.
19. Fremeau Jr RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
20. Gao W, Chen G, Reinert KC, Ebner TJ (2006) Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. J Neurosci 26: 8377-8387.
21. Gincel D, Regan MR, Jin L, Watkins AM, Bergles DE, Rothstein JD (2007) Analysis of cerebellar Purkinje cells using EAAT4 glutamate transporter promoter reporter in mice generated via bacterial artificial chromosome-mediated transgenesis. Exp Neurol 203:205-212.
22. Hansel C, Linden DJ, D'Angelo E (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4:467-475.
23. Hawkes R, Gravel C (1991) The modular cerebellum. Prog Neurobiol 36:309-327.
24. Huang YH, Bergles DE (2004) Glutamate transporters bring competition to the synapse. Curr Opin Neurobiol 14:346-352.
25. Huang YH, Dykes-Hoberg M, Tanaka K, Rothstein JD, Bergles DE (2004) Climbing fiber activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J Neurosci 24:103-111. (Pubitemid 38181675)
26. Huang YH, Sinha SR, Fedoryak OD, Ellis-Davies GC, Bergles DE (2005) Synthesis and characterization of 4-methoxy-7-nitroindolinyl-Daspartate, a caged compound for selective activation of glutamate transporters and N-methyl-D-aspartate receptors in brain tissue. Biochemistry 44:3316-3326. (Pubitemid 40322002)
27. Ito M, KanoM (1982) Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett 33:253-258.
28. Khaliq ZM, Raman IM (2005) Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J Neurosci 25:454-463.
29. Kitazawa S, Kimura T, Yin PB (1998) Cerebellar complex spikes encode both destinations and errors in arm movement. Nature 392:494-497. (Pubitemid 28169870)
30. Lang EJ, Sugihara I, Welsh JP, Llinas R (1999) Patterns of spontaneous Purkinje cell complex spike activity in the awake rat. J Neurosci 19:2728-2739. (Pubitemid 29162420)
31. Liu G, Choi S, Tsien RW (1999) Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22:395-409. (Pubitemid 29109672)
32. Llinas R, Baker R, Sotelo C (1974) Electrotonic coupling between neurons in cat inferior olive. J Neurophysiol 37:560-571.
33. Llinas R, Walton K, Hillman DE, Sotelo C (1975) Inferior olive: its role in motor learning. Science 190:1230-1231.
34. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M (2001) Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475. (Pubitemid 32778564)
35. Mathy A, Ho SS, Davie JT, Duguid IC, Clark BA, HäusserM (2009) Encoding of oscillations by axonal bursts in inferior olive neurons. Neuron 62:388-399.
36. Miledi R (1966) Strontium as a substitute for calcium in the process of transmitter release at the neuromuscular junction. Nature 212:1233-1234.
37. Moechars D, Weston MC, Leo S, Callaerts-Vegh Z, Goris I, Daneels G, Buist A, Cik M, van der Spek P, Kass S, Meert T, D'Hooge R, Rosenmund C, Hampson RM (2006) Vesicular glutamate transporter vGluT2 expression levels control quantal size and neuropathic pain. J Neurosci 26:12055-12066.
38. Monsivais P, Clark BA, Roth A, Hausser M (2005) Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci 25:464-472. (Pubitemid 40105617)
39. Nikkuni O, Takayasu Y, Iino M, Tanaka K, Ozawa S (2007) Facilitated activation of metabotropic glutamate receptors in cerebellar Purkinje cells in glutamate transporter EAAT4-deficient mice. Neurosci Res 59:296-303. (Pubitemid 47503379)
40. Nusser Z, Mulvihill E, Streit P, Somogyi P (1994) Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61:421-427. (Pubitemid 24240291)
41. O'Hearn E, Molliver ME (1997) The olivocerebellar projection mediates ibogaine-induced degeneration of Purkinje cells: a model of indirect, trans-synaptic excitotoxicity. J Neurosci 17:8828-8841. (Pubitemid 27481748)
42. Oliet SH, Malenka RC, Nicoll RA (1996) Bidirectional control of quantal size by synaptic activity in the hippocampus. Science 271:1294-1297.
43. Otis TS, Kavanaugh MP, Jahr CE (1997) Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277:1515-1518.
44. Ozden I, Sullivan MR, Lee HM, Wang SS (2009) Reliable coding emerges from coactivation of climbing fibers in microbands of cerebellar Purkinje neurons. J Neurosci 29:10463-10473.
45. Ozol K, Hayden JM, Oberdick J, Hawkes R (1999) Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol 412:95-111. (Pubitemid 29380327)
46. Palkovits M, Mezey E, Hamori J, Szentagothai J (1977) Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses. Exp Brain Res 28:189-209.
47. Safo PK, Cravatt BF, Regehr WG (2006) Retrograde endocannabinoid signaling in the cerebellar cortex. Cerebellum 5:134-145.
48. Sasaki K, Bower JM, Llinas R (1989) Multiple Purkinje cell recording in rodent cerebellar cortex. Eur J Neurosci 1:572-586.
49. Shen Y, Linden DJ (2005) Long-term potentiation of neuronal glutamate transporters. Neuron 46:715-722. (Pubitemid 40733127)
50. Sugihara I, Wu HS, Shinoda Y (2001) The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J Neurosci 21:7715-7723. (Pubitemid 32904970)
51. Sugihara I, Marshall SP, Lang EJ (2007) Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in crus IIa of the rat cerebellar cortex. J Comp Neurol 501:13-29. (Pubitemid 46155870)
52. Sugihara I, Fujita H, Na J, Quy PN, Li BY, Ikeda D (2009) Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. J Comp Neurol 512:282-304.
53. Szapiro G, Barbour B (2007) Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat Neurosci 10:735-742. (Pubitemid 46828513)
54. Takayasu Y, Iino M, Kakegawa W, Maeno H, Watase K, Wada K, Yanagihara D, Miyazaki T, Komine O, Watanabe M, Tanaka K, Ozawa S (2005) Differential roles of glial and neuronal glutamate transporters in Purkinje cell synapses. J Neurosci 25:8788-8793.
55. Telgkamp P, Raman IM (2002) Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22:8447-8457.
56. Telgkamp P, Padgett DE, Ledoux VA, Woolley CS, Raman IM (2004) Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41:113-126.
57. Wadiche JI, Jahr CE (2001) Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32:301-313.
58. Wadiche JI, Jahr CE (2005) Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat Neurosci 8:1329-1334.
59. Wadiche JI, Tzingounis AV, Jahr CE (2006) Intrinsic kinetics determine the time course of neuronal synaptic transporter currents. Proc Natl Acad Sci U S A 103:1083-1087.
60. Wang SSH, Denk W, Häusser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266-1273.
61. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, Erickson JD, Liu G (2005) Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25:622-6234.
62. Xu-Friedman MA, RegehrWG (2000) Probing fundamental aspects of synaptic transmission with strontium. J Neurosci 20:4414-4422.
63. Yang Y, Gozen O, Watkins A, Lorenzini I, Lepore A, Gao Y, Vidensky S, Brennan J, Poulsen D,WonPark J, Li Jeon N, Robinson MB, Rothstein JD (2009) Presynaptic regulation of astroglial excitatory neurotransmitter transporter GLT1. Neuron 61:880-894.