Ectopic release sites lack fast vesicle recycling mechanisms, causing long-term depression of neuron-glial transmission in rat cerebellum

GLIA

Volumn 59, Issue 1, 2011, Pages 82-93

  Balakrishnan, Saju ^a   Jackson, Claire ^a   Russell, Noah ^b   Bellamy, Tomas C ^a,c  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Bergmann glial cell; Purkinje neuron; Synaptic plasticity; Vesicle recycling

Indexed keywords

AMPA RECEPTOR; CALCIUM;

ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CEREBELLUM; EX VIVO STUDY; GLIA CELL; LONG TERM DEPRESSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT;

ANIMALS; CELL COMMUNICATION; CEREBELLUM; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; LONG-TERM SYNAPTIC DEPRESSION; NEUROGLIA; NEURONS; RATS; RATS, WISTAR; SYNAPTIC VESICLES;

EID: 78349257761     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21078     Document Type: Article

References (43)

1. Allen NJ, Barres BA. 2005. Signaling between glia and neurons: Focus on synaptic plasticity. Curr Opin Neurobiol 15: 542-548.
2. Balakrishnan S, Bellamy TC. 2009. Depression of parallel and climbing fiber transmission to Bergmann glia is input specific and correlates with increased precision of synaptic transmission. Glia 57: 393-401.
3. Bellamy TC. 2007. Presynaptic modulation of parallel fibre signalling to Bergmann glia. Neuropharmacology 52: 368-375.
4. Bellamy TC, Ogden D. 2005. Short-term plasticity of Bergmann glial cell extrasynaptic currents during parallel fibre stimulation in rat cerebellum. Glia 52: 325-335.
5. Bellamy TC, Ogden D. 2006. Long-term depression of neuron to glial signalling in rat cerebellar cortex. Eur J Neurosci 23: 581-586.
6. Chadderton P, Margrie TW, Hausser M. 2004. Integration of quanta in cerebellar granule cells during sensory processing. Nature 428: 856-860.
7. 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.
8. Dittman JS, Regehr WG. 1997. Mechanism and kinetics of heterosynaptic depression at a cerebellar synapse. J Neurosci 17: 9048-9059.
9. Grosche J, Kettenmann H, Reichenbach A. 2002. Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neurosci Res 68: 138-149.
10. 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.
11. Hirrlinger J, Hulsmann S, Kirchhoff F. 2004. Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur J Neurosci 20: 2235-2239.
12. 2+-permeable AMPA receptors in Bergmann glia. Science 292: 926-929.
13. Isope P, Barbour B. 2002. Properties of unitary granule cell → Purkinje cell synapses in adult rat cerebellar slices. J Neurosci 22: 9668-9678.
14. Ito M. 2002. The molecular organization of cerebellar long-term depression. Nat Rev Neurosci 3: 896-902.
15. Jordan R, Lemke EA, Klingauf J. 2005. Visualization of synaptic vesicle movement in intact synaptic boutons using fluorescence fluctuation spectroscopy. Biophys J 89: 2091-102.
16. Jorntell H, Ekerot C. 2006. Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci 26: 11786-11797.
17. Jorntell H, Hansel C. 2006. Synaptic memories upside down: Bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron 52: 227-238.
18. Kreitzer AC, Regehr WG. 2000. Modulation of transmission during trains at a cerebellar synapse. J Neurosci 20: 1348-1357.
19. Kuromi H, Kidokoro Y. 1998. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20: 917-925.
20. 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.
21. Mathy A, Ho SS, Davie JT, Duguid IC, Clark BA, Hausser M. 2009. Encoding of oscillations by axonal bursts in inferior olive neurons. Neuron 62: 388-399.
22. Matsui K, Jahr CE. 2003. Ectopic release of synaptic vesicles. Neuron 40: 1173-1183.
23. Matsui K, Jahr CE. 2004. Differential control of synaptic and ectopic vesicular release of glutamate. J Neurosci 24: 8932-8939.
24. Matsui K, Jahr CE. 2006. Exocytosis unbound. Curr Opin Neurobiol 16: 305-311.
25. Matsui K, Jahr CE, Rubio ME. 2005. High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release. J Neurosci 25: 7538-7547.
26. Muller T, Moller T, Berger T, Schnitzer J, Kettenmann H. 1992. Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells [published erratum appears in Science 1992;257:1190]. Science 256: 1563-1566.
27. Muller T, Moller T, Neuhaus J, Kettenmann H. 1996. Electrical coupling among Bergmann glial cells and its modulation by glutamate receptor activation. Glia 17: 274-284.
28. Neale SA, Garthwaite J, Batchelor AM. 2001. Metabotropic glutamate receptor subtypes modulating neurotransmission at parallel fibre-Purkinje cell synapses in rat cerebellum. Neuropharmacology 41: 42-49.
29. Neher E, Sakaba T. 2008. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872.
30. Oliet SH, Piet R, Poulain DA. 2001. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292: 923-926.
31. Pyott SJ, Rosenmund C. 2002. The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons. J Physiol 539: 523-535.
32. Rizo J, Rosenmund C. 2008. Synaptic vesicle fusion. Nat Struct Mol Biol 15: 665-674.
33. Rizzoli SO, Betz WJ. 2005. Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69.
34. Ryan TA. 1999. Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci 19: 1317-1323.
35. Safo PK, Cravatt BF, Regehr WG. 2006. Retrograde endocannabinoid signaling in the cerebellar cortex. Cerebellum 5: 134-145.
36. Sakaba T, Neher E. 2001. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131.
37. Shen Y, Linden DJ. 2005. Long-term potentiation of neuronal glutamate transporters. Neuron 46: 715-722.
38. Shin JH, Linden DJ. 2005. An NMDA receptor/nitric oxide cascade is involved in cerebellar LTD but is not localized to the parallel fiber terminal. J Neurophysiol 94: 4281-4289.
39. Sudhof TC. 2004. The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547.
40. Tokuoka H, Goda Y. 2006. Myosin light chain kinase is not a regulator of synaptic vesicle trafficking during repetitive exocytosis in cultured hippocampal neurons. J Neurosci 26: 11606-11614.
41. 2+ channels determines fast neurotransmitter release. Neuron 53: 563-575.
42. Wu LG, Ryan TA, Lagnado L. 2007. Modes of vesicle retrieval at ribbon synapses, calyx-type synapses, and small central synapses. J Neurosci 27: 11793-11802.
43. Zucker RS, Regehr WG. 2002. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.