Quantitative organization of GABAergic synapses in the molecular layer of the mouse cerebellar cortex

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Briatore, Federica ^a   Patrizi, Annarita ^a   Viltono, Laura ^a   Sassoe Pognetto, Marco ^a   Wulff, Peer ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; ALPHA DYSTROGLYCAN; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ANTIBODY; DYSTROGLYCAN; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CEREBELLUM CORTEX; CONTROLLED STUDY; GABAERGIC TRANSMISSION; GENE DELETION; IMMUNOREACTIVITY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NERVE FIBER; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PURKINJE CELL; QUANTITATIVE ANALYSIS; STELLATE CELL; SYNAPTIC INHIBITION; SYNAPTOGENESIS; ANIMAL; CYTOLOGY; ENZYME SPECIFICITY; GENE INACTIVATION; GENETICS; IMMUNOLOGY; METABOLISM; NERVE CELL; SYNAPSE;

ANIMALS; ANTIBODIES; CEREBELLAR CORTEX; DYSTROGLYCANS; GAMMA-AMINOBUTYRIC ACID; GENE KNOCKOUT TECHNIQUES; MICE; NEURONS; PROTEIN SUBUNITS; PURKINJE CELLS; RECEPTORS, GABA-A; SEQUENCE DELETION; SUBSTRATE SPECIFICITY; SYNAPSES;

EID: 77957877360     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012119     Document Type: Article

References (69)

1. Ramón, Cajal S (1911) Histologie du système nerveux de l'homme et des vertébrés, vol.II. Paris: Maloine.
2. Fox FA, Hillman DE, Sugesmund KA, Dutta CR (1967) The primate cerebellar cortex: A Golgi and electron microscope study. Prog Brain Res 25: 174-225.
3. Palay S, Chan-Palay V (1974) Cerebellar Cortex: Cytology and Organization. Berlin: Springer.
4. Eccles J, Ito M, Szentagothai J (1967) The Cerebellum as a Neuronal Machine. Berlin: Springer.
5. Marr D (1969) A theory of cerebellar cortex. J Physiol 202: 437-470.
6. Albus J (1971) A theory of cerebellar function. Math Biosci 10: 25-61.
7. Ito M (1984) The Cerebellum and Neural Control. New York: Raven Press.
8. Ito M (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78: 272-303.
9. Sotelo C (2004) Cellular and genetic regulation of the development of the cerebellar system. Prog Neurobiol 72: 295-339.
10. Nakanishi S (2005) Synaptic mechanisms of the cerebellar cortical network. Trends Neurosci 28: 93-100.
11. Rokni D, Llinas R, Yarom Y (2008) The Morpho/Functional Discrepancy in the Cerebellar Cortex: Looks Alone are Deceptive. Front Neurosci 2: 192-198.
12. Harvey RJ, Napper RM (1991) Quantitative studies on the mammalian cerebellum. Prog Neurobiol 36: 437-463.
13. th edition. New York: Oxford UP. pp 271-309.
14. Sultan F, Bower JM (1998) Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis. J Comp Neurol 393: 353-373.
15. Schilling K, Oberdick J, Rossi F, Baader SL (2008) Besides Purkinje cells and granule neurons: an appraisal of the cell biology of the interneurons of the cerebellar cortex. Histochem Cell Biol 130: 601-615.
16. Mittmann W, Koch U, Háusser M (2005) Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J Physiol 563: 369-378.
17. Wulff P, Schonewille M, Renzi M, Viltono L, Sassoe-Pognetto M, et al. (2009) Role of GABAergic interneurons in cerebellar motor learning. Nat Neurosci 12: 1042-1049.
18. Llano I, Gerschenfeld HM (1993) Inhibitory synaptic currents in stellate cells of rat cerebellar slices. J Physiol 468: 177-200.
19. Kondo S, Marty A (1998) Synaptic currents at individual connections among stellate cells in rat cerebellar slices. J Physiol 509: 221-232.
20. Chavas J, Marty A (2003) Coexistence of excitatory and inhibitory GABA synapses in the cerebellar interneuron network. J Neurosci 23: 2019-2031.
21. Jaeger D, De Schutter E, Bower JM (1997) The role of synaptic and voltage-gated currents in the control of Purkinje cell spiking: a modeling study. J Neurosci 17: 91-106.
22. Medina JF, Garcia KS, Nores WL, Taylor NM, Mauk MD (2000) Timing mechanisms in the cerebellum: testing predictions of a large-scale computer simulation. J Neurosci 20: 5516-5525.
23. Santamaria F, Jaeger D, De Schutter E, Bower JM (2002) Modulatory effects of parallel fiber and molecular layer interneuron synaptic activity on Purkinje cell responses to ascending segment input: a modeling study. J Comput Neurosci 13: 217-235.
24. Santamaria F, Tripp PG, Bower JM (2007) Feedforward inhibition controls the spread of granule cell-induced Purkinje cell activity in the cerebellar cortex. J Neurophysiol 97: 248-263.
25. Solinas S, Maex R, De Schutter E (2003) Synchronization of Purkinje cell pairs along the parallel fiber axis: a model. Neurocomputing 52-54+97-102.
26. Sieghart W, Sperk G (2002) Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr Top Med Chem 2: 795-816.
27. Rudolph U, Möhler H (2006) GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr Opin Pharmacol 6: 18-23.
28. Pöltl A, Hauer B, Fuchs K, Tretter V, Sieghart W (2003) Subunit composition and quantitative importance of GABA(A) receptor subtypes in the cerebellum of mouse and rat. J Neurochem 87: 1444-1455.
29. Sassoe-Pognetto M, Panzanelli P, Sieghart W, Fritschy J-M (2000) Co-localization of multiple GABAA receptor subtypes with gephyrin at postsynaptic sites. J Comp Neurol 420: 481-498.
30. Laurie DJ, Seeburg PH, Wisden W (1992) The distribution of 13 GABAA receptor subunit mRNAs in the rat brain. II. Olfactory bulb and cerebellum. J Neurosci 12: 1063-1076.
31. Fritschy JM, Panzanelli P (2006) Molecular and synaptic organization of GABAA receptors in the cerebellum: Effects of targeted subunit gene deletions. Cerebellum 5: 275-285.
32. Fritschy JM, Panzanelli P, Kralic JE, Vogt K, Sassoe-Pognetto M (2006) Differential dependence of axo-dendritic and axo-somatic GABAergic synapses on GABAA receptors containing the a1 subunit in Purkinje cells. J Neurosci 26: 3245-3255.
33. Patrizi A, Scelfo B, Viltono L, Briatore F, Fukaya M, et al. (2008) Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc Natl Acad Sci USA 105: 13151-13156.
34. Viltono L, Patrizi A, Fritschy JM, Sassoe-Pognetto M (2008) Synaptogenesis in the cerebellar cortex: Differential regulation of gephyrin and GABAA receptors at somatic and dendritic synapses of Purkinje cells. J Comp Neurol 508: 579-591.
35. Kralic JE, Sidler C, Parpan F, Homanics GE, Morrow AL, et al. (2006) Compensatory alteration of inhibitory synaptic circuits in cerebellum and thalamus of gamma-aminobutyric acid type A receptor alpha1 subunit knockout mice. J Comp Neurol 495: 408-421.
36. Vicini S, Ferguson C, Prybylowski K, Kralic J, Morrow AL, et al. (2001) GABA(A) receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21: 3009-3016.
37. Barski JJ, Dethleffsen K, Meyer M (2000) Cre recombinase expression in cerebellar Purkinje cells. Genesis 28: 93-98.
38. Gao B, Fritschy JM, Benke D, Mohler H (1993) Neuron-specific expression of GABAA-receptor subtypes: differential association of the alpha 1- and alpha 3-subunits with serotonergic and GABAergic neurons. Neuroscience 54: 881-892.
39. Benke D, Honer M, Michel C, Mohler H (1996) GABAA receptor subtypes differentiated by their g-subunit variants: prevalence, pharmacology and subunit architecture. Neuropharmacology 35: 1413-1423.
40. Gunther U, Benson J, Benke D, Fritschy JM, Reyes G, et al. (1995) Benzodiazepine-insensitive mice generated by targeted disruption of the c2 subunit gene of c-aminobutyric acid type A receptors. Proc Natl Acad Sci USA 92: 7749-7753.
41. Yee BK, Keist R, von Boehmer L, Studer R, Benke D, et al. (2005) A schizophrenia-related sensorimotor deficit links a3-containing GABAA receptors to a dopamine hyperfunction. Proc Natl Acad Sci USA 102: 17154-17159.
42. Varoqueaux F, Jamain S, Brose N (2004) Neuroligin 2 is exclusively localized to inhibitory synapses. Eur J Cell Biol 83: 449-456.
43. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345: 315-319.
44. Lévi S, Grady RM, Henry MD, Campbell KP, Sanes JR, et al. (2002) Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J Neurosci 22: 4274-4285.
45. Celio M (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375-475.
46. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, et al. (1997) Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94: 1488-1493.
47. Schneider Gasser EM, Straub CJ, Panzanelli P, Weinmann O, Sassoe-Pognetto M, et al. (2006) Immunofluorescence in brain sections: simultaneous detection of pre- and postsynaptic proteins in identified neurons. Nat Protocols 1: 1887-1897.
48. Howard CV, Reed MG (2005) Unbiased Stereology. Oxford: BIOS Scientific Publisher.
49. Phend KD, Weinberg RJ, Rustioni A (1992) Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J Histochem Cytochem 40: 1011-1020.
50. Knuesel I, Mastrocola M, Zuellig RA, Bornhauser B, Schaub MC, et al. (1999) Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur J Neurosci 11: 4457-4462.
51. Grady RM, Wozniak DF, Ohlemiller KK, Sanes JR (2006) Cerebellar synaptic defects and abnormal motor behavior in mice lacking alpha- and beta-dystrobrevin. J Neurosci 26: 2841-2851.
52. Stell BM, Rostaing P, Triller A, Marty A (2007) Activation of presynaptic GABA(A) receptors induces glutamate release from parallel fiber synapses. J Neurosci 27: 9022-9031.
53. Nusser Z, Cull-Candy S, Farrant M (1997) Differences in synaptic GABA(A) receptor number underlie variation in GABA mini amplitude. Neuron 19: 697-709.
54. Barmack NH, Yakhnitsa V (2008) Functions of interneurons in mouse cerebellum. J Neurosci 28: 1140-1152.
55. Sillitoe RV, Chung SH, Fritschy JM, Hoy M, Hawkes R (2008) Golgi cell dendrites are restricted by Purkinje cell stripe boundaries in the adult mouse cerebellar cortex. J Neurosci 28: 2820-2826.
56. Dieudonné S, Dumoulin A (2000) Serotonin-driven long-range inhibitory connections in the cerebellar cortex. J Neurosci 20: 1837-1848.
57. Dumoulin A, Triller A, Dieudonné S (2001) IPSC kinetics at identified GABAergic and mixed GABAergic and glycinergic synapses onto cerebellar Golgi cells. J Neurosci 21: 6045-6057.
58. Dean I, Robertson SJ, Edwards FA (2003) Serotonin drives a novel GABAergic synaptic current recorded in rat cerebellar Purkinje cells: a Lugaro cell to Purkinje cell synapse. J Neurosci 23: 4457-4469.
59. Lainé J, Axelrad H (2002) Extending the cerebellar Lugaro cell class. Neuroscience 115: 363-374.
60. Korbo L, Andersen BB, Ladefoged O, Møller A (1993) Total numbers of various cell types in rat cerebellar cortex estimated using an unbiased stereological method. Brain Res 609: 262-268.
61. Jakovcevski I, Siering J, Hargus G, Karl N, Hoelters L, et al. (2009) Close homologue of adhesion molecule L1 promotes survival of Purkinje and granule cells and granule cell migration during murine cerebellar development. J Comp Neurol 513: 496-510.
62. Llano I, Marty A (1995) Presynaptic metabotropic glutamatergic regulation of inhibitory synapses in rat cerebellar slices. J Physiol 486: 163-176.
63. Jörntell H, Ekerot CF (2002) Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron 34: 797-806.
64. Smith SL, Otis TS (2005) Pattern-dependent, simultaneous plasticity differentially transforms the input-output relationship of a feedforward circuit. Proc Natl Acad Sci USA 102: 14901-14906.
65. Mittmann W, Hausser M (2007) Linking synaptic plasticity and spike output at excitatory and inhibitory synapses onto cerebellar Purkinje cells. J Neurosci 27: 5559-5570.
66. Scelfo B, Sacchetti B, Strata P (2008) Learning-related long-term potentiation of inhibitory synapses in the cerebellar cortex. Proc Natl Acad Sci U S A 105: 769-774.
67. Wulff P, Goetz T, Leppa E, Linden AM, Renzi M, et al. (2007) From synapse to behavior: rapid modulation of defined neuronal types with engineered GABAA receptors. Nat Neurosci 10: 923-929.
68. Maex R, De Schutter E (2003) Resonant synchronization in heterogeneous networks of inhibitory neurons. J Neurosci 23: 10503-10514.
69. Maex R, De Schutter E (2005) Oscillations in the cerebellar cortex: a prediction of their frequency bands. Prog Brain Res 148: 181-188.