Target-dependent use of coreleased inhibitory transmitters at central synapses

Journal of Neuroscience

Volumn 25, Issue 28, 2005, Pages 6490-6498

  Dugué, Guillaume P ^a   Dumoulin, Andréa ^a   Triller, Antoine ^a   Dieudonné, Stéphane ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

Cerebellum; Corelease; GABA; Glycine; Inhibition; Vestibular system

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; GLYCINE; GLYCINE RECEPTOR; NEUROTRANSMITTER; 3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; PYRIDAZINE DERIVATIVE; STRYCHNINE;

ANIMAL TISSUE; ARTICLE; BRUSH BORDER; CELL COMMUNICATION; CELL CONTACT; CONTROLLED STUDY; GOLGI COMPLEX; GRANULE CELL; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; INTERNEURON; NERVE ENDING; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; TARGET CELL; VESTIBULAR SYSTEM; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; CEREBELLUM CORTEX; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG ANTAGONISM; EVOKED RESPONSE; FLUORESCENCE MICROSCOPY; PATCH CLAMP; PHYSIOLOGY; SECRETION; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CEREBELLAR CORTEX; EVOKED POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLYCINE; INTERNEURONS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; PYRIDAZINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, GLYCINE; STRYCHNINE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 22244485980     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1500-05.2005     Document Type: Article

References (79)

1. Awatramani GB, Turecek R, Trussell LO (2005) Staggered development of GABAergic and glycinergic transmission in the MNTB. J Neurophysiol 93:819-828.
2. Beierlein M, Gibson JR, Connors BW (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3:904-910.
3. Blitz DM, Nusbaum MP (1999) Distinct functions for cotransmitters mediating motor pattern selection. J Neurosci 19:6774-6783.
4. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau Jr RT, Edwards RH, Storm-Mathisen J, Chaudhry FA (2004) Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480:264-280.
5. Burnstock G (2004) Cotransmission. Curr Opin Pharmacol 4:47-52.
6. Chadderton P, Margrie TW, Hausser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860.
7. A receptor-mediated IPSCs in identified lamina I neurons of the adult rat spinal cord. J Neurosci 19:7342-7355.
8. Coggeshall RE, Carlton SM (1997) Receptor localization in the mammalian dorsal horn and primary afferent neurons. Brain Res Brain Res Rev 24:28-66.
9. Dieudonne S (1995) Glycinergic synaptic currents in Golgi cells of the rat cerebellum. Proc Natl Acad Sci USA 92:1441-1445.
10. Dino MR, Nunzi MG, Anelli R, Mugnaini E (2000) Unipolar brush cells of the vestibulocerebellum: afferents and targets. Prog Brain Res 124:123-137.
11. Dumba JS, Irish PS, Anderson NL, Westrum LE (1998) Electron microscopic analysis of gamma-aminobutyric acid and glycine colocalization in rat trigeminal subnucleus caudalis. Brain Res 806:16-25.
12. Dumoulin A, Rostaing P, Bedet C, Levi S, Isambert MF, Henry JP, Triller A, Gasnier B (1999) Presence of the vesicular inhibitory amino acid transporter in GABAergic and glycinergic synaptic terminal boutons. J Cell Sci 112:811-823.
13. Dumoulin A, Triller A, Dieudonne S (2001) IPSC kinetics at identified GABAergic and mixed GABAergic and glycinergic synapses onto cerebellar Golgi cells. J Neurosci 21:6045-6057.
14. A receptor-mediated transmission at newly formed Golgi-granule cell synapses in the cerebellum. Neuropharmacology 44:181-189.
15. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402:72-75.
16. Galarreta M, Erdelyi F, Szabo G, Hestrin S (2004) Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 24:9770-9778.
17. Gao BX, Stricker C, Ziskind-Conhaim L (2001) Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J Neurophysiol 86:492-502.
18. Geiman EJ, Knox MC, Alvarez FJ (2000) Postnatal maturation of gephyrin/glycine receptor clusters on developing Renshaw cells. J Comp Neurol 426:130-142.
19. Geurts FJ, De Schutter E, Dieudonne S (2003) Unraveling the cerebellar cortex: cytology and cellular physiology of large-sized interneurons in the granular layer. Cerebellum 2:290-299.
20. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
21. Gillespie DC, Kim G, Kandler K (2005) Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci 8:332-338.
22. A, glycine receptor, and mixed synaptic currents in renshaw cells and ventral spinal interneurons. J Neurosci 25:2010-2023.
23. Gutierrez R (2003) The GABAergic phenotype of the " glutamatergic" granule cells of the dentate gyrus. Prog Neurobiol 71:337-358.
24. Harvey RJ, Depner UB, Wassle H, Ahmadi S, Heindl C, Reinold H, Smart TG, Harvey K, Schutz B, Abo-Salem OM, Zimmer A, Poisbeau P, Welzl H, Wolfer DP, Betz H, Zeilhofer HU, Muller U (2004) GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science 304:884-887.
25. Hosie AM, Dunne EL, Harvey RJ, Smart TG (2003) Zinc-mediated inhibition of GABA(A) receptors: discrete binding sites underlie subtype specificity. Nat Neurosci 6:362-369.
26. Hu EH, Bloomfield SA (2003) Gap junctional coupling underlies the short-latency spike synchrony of retinal α ganglion cells. J Neurosci 23:6768-6777.
27. Jan LY, Jan YN (1982) Peptidergic transmission in sympathetic ganglia of the frog. J Physiol (Lond) 327:219-246.
28. Jo YH, Schlichter R (1999) Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci 2:241-245.
29. Jo YH, Stoeckel ME, Schlichter R (1998) Electrophysiological properties of cultured neonatal rat dorsal horn neurons containing GABA and metenkephalin-like immunoreactivity. J Neurophysiol 79:1583-1586.
30. Jonas P, Bischofberger J, Sandkuhler J (1998) Corelease of two fast neurotransmitters at a central synapse. Science 281:419-424.
31. Kaneda M, Farrant M, Cull-Candy SG (1995) Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J Physiol (Lond) 485:419-435.
32. Kao YH, Lassova L, Bar-Yehuda T, Edwards RH, Sterling P, Vardi N (2004) Evidence that certain retinal bipolar cells use both glutamate and GABA. J Comp Neurol 478:207-218.
33. Katz PS, Harris-Warrick RM (1989) Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. 11. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. J Neurophysiol 62:571-581.
34. Keller AF, Coull JA, Chery N, Poisbeau P, De Koninck Y (2001) Region-specific developmental specialization of GABA-glycine cosynapses in laminas I-II of the rat spinal dorsal horn. J Neurosci 21:7871-7880.
35. A miniature IPSCs in lamina II of the spinal cord. J Neurosci 24:907-915.
36. Korada S, Schwartz IR (1999) Development of GABA, glycine, and their receptors in the auditory brainstem of gerbil: a light and electron microscopic study. J Comp Neurol 409:664-681.
37. Kotak VC, Korada S, Schwartz IR, Sanes DH (1998) A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18:4646-4655.
38. Laube B, Kuhse J, Rundstrom N, Kirsch J, Schmieden V, Betz H (1995) Modulation by zinc ions of native rat and recombinant human inhibitory glycine receptors. J Physiol (Lond) 483:613-619.
39. Li J, Perl ER (1995) ATP modulation of synaptic transmission in the spinal substantia gelatinosa. J Neurosci 15:3357-3365.
40. Li WC, Soffe SR, Roberts A (2004) Glutamate and acetylcholine corelease at developing synapses. Proc Natl Acad Sci USA 101:15488-15493.
41. Li YV, Hough CJ, Sarvey JM (2003) Do we need zinc to think? Sci STKE 2003:pe19.
42. Long MA, Landisman CE, Connors BW (2004) Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J Neurosci 24:341-349.
43. Malcangio M, Bowery NG (1996) GABA and its receptors in the spinal cord. Trends Pharmacol Sci 17:457-462.
44. Mann-Metzer P, Yarom Y (1999) Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J Neurosci 19:3298-3306.
45. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870-876.
46. Morin F, Dino MR, Mugnaini E (2001) Postnatal differentiation of unipolar brush cells and mossy fiber-unipolar brush cell synapses in rat cerebellum. Neuroscience 104:1127-1139.
47. Moss SJ, Smart TG (2001) Constructing inhibitory synapses. Nat Rev Neurosci 2:240-250.
48. Mugnaini E, Floris A (1994) The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. J Comp Neurol 339:174-180.
49. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H (2004) Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7:17-23.
50. Nishimaru H, Restrepo CE, Ryge J, Yanagawa Y, Kiehn O (2005) Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc Natl Acad Sci USA 102:5245-5249.
51. Nunzi MG, Shigemoto R, Mugnaini E (2002) Differential expression of calretinin and metabotropic glutamate receptor mGluR1alpha defines subsets of unipolar brush cells in mouse cerebellum. J Comp Neurol 451:189-199.
52. Nunzi MG, Russo M, Mugnaini E (2003) Vesicular glutamate transporters VGLUT1 and VGLUT2 define two subsets of unipolar brush cells in organotypic cultures of mouse vestibulocerebellum. Neuroscience 122:359-371.
53. O'Brien JA, Berger AJ (1999) Cotransmission of GABA and glycine to brain stem motoneurons. J Neurophysiol 82:1638-1641.
54. A receptor α 1 subunit influences inhibitory synaptic transmission to motoneurons within a motor nucleus. J Neurosci 21:8482-8494.
55. Ornung G, Shupliakov O, Ottersen OP, Storm-Mathisen J, Cullheim S (1994) Immunohistochemical evidence for coexistence of glycine and GABA in nerve terminals on cat spinal motoneurones: an ultrastructural study. NeuroReport 5:889-892.
56. Ottem EN, Godwin JG, Krishnan S, Petersen SL (2004) Dual-phenotype GABA/glutamate neurons in adult preoptic area: sexual dimorphism and function. J Neurosci 24:8097-8105.
57. Ottersen OP, Storm-Mathisen J, Somogyi P (1988) Colocalization of glycine-like and GABA-like immunoreactivities in Golgi cell terminals in the rat cerebellum: a postembedding light and electron microscopic study. Brain Res 450:342-353.
58. A receptors and glomerular geometry. Neuron 20:783-795.
59. Rossi DJ, Alford S, Mugnaini E, Slater NT (1995) Properties of transmission at a giant glutamatergic synapse in cerebellum: the mossy fiber-unipolar brush cell synapse. J Neurophysiol 74:24-42.
60. Russier M, Kopysova IL, Ankri N, Ferrand N, Debanne D (2002) GABA and glycine co-release optimizes functional inhibition in rat brainstem motoneurons in vitro. J Physiol (Lond) 541:123-137.
61. Sagne C, El Mestikawy S, Isambert MF, Hamon M, Henry JP, Giros B, Gasnier B (1997) Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases. FEBS Lett 417:177-183.
62. Schneider SP, Fyffe RE (1992) Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. J Neurophysiol 68:397-406.
63. Sekerkova G, Ilijic E, Mugnaini E (2004) Time of origin of unipolar brush cells in the rat cerebellum as observed by prenatal bromodeoxyuridine labeling. Neuroscience 127:845-858.
64. Shupliakov O, Ornung G, Brodin L, Ulfhake B, Ottersen OP, Storm-Mathisen J, Cullheim S (1993) Immunocytochemical localization of amino acid neurotransmitter candidates in the ventral horn of the cat spinal cord: a light microscopic study. Exp Brain Res 96:404-418.
65. Smith AJ, Owens S, Forsythe ID (2000) Characterisation of inhibitory and excitatory postsynaptic currents of the rat medial superior olive. J Physiol (Lond) 529:681-698.
66. Sossin WS, Sweet-Cordero A, Scheller RH (1990) Dale's hypothesis revisited: different neuropeptides derived from a common prohormone are targeted to different processes. Proc Natl Acad Sci USA 87:4845-4848.
67. Suwa H, Saint-Amant L, Triller A, Drapeau P, Legendre P (2001) High-affinity zinc potentiation of inhibitory postsynaptic glycinergic currents in the zebrafish hindbrain. J Neurophysiol 85:912-925.
68. Swensen AM, Golowasch J, Christie AE, Coleman MJ, Nusbaum MP, Marder E (2000) GABA and responses to GABA in the stomatogastric ganglion of the crab Cancer borealis. J Exp Biol 203:2075-2092.
69. Taal W, Holstege JC (1994) GABA and glycine frequently colocalize in terminals on cat spinal motoneurons. NeuroReport 5:2225-2228.
70. Tanaka I, Ezure K (2004) Overall distribution of GLYT2 mRNA-containing versus GAD67 mRNA-containing neurons and colocalization of both mRNAs in midbrain, pons, and cerebellum in rats. Neurosci Res 49:165-178.
71. Thirumalai V, Marder E (2002) Colocalized neuropeptides activate a central pattern generator by acting on different circuit targets. J Neurosci 22:1874-1882.
72. Todd AJ (1990) An electron microscope study of glycine-like immunoreactivity in laminae I-III of the spinal dorsal horn of the rat. Neuroscience 39:387-394.
73. Todd AJ, Watt C, Spike RC, Sieghart W (1996) Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci 16:974-982.
74. Vincent P, Marty A (1993) Neighboring cerebellar Purkinje cells communicate via retrograde inhibition of common presynaptic interneurons. Neuron 11:885-893.
75. Walker MC, Ruiz A, Kullmann DM (2001) Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses. Neuron 29:703-715.
76. Wall MJ, Usowicz MM (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9:533-548.
77. Wang Z, Li JY, Dahlstrom A, Danscher G (2001) Zinc-enriched GABAergic terminals in mouse spinal cord. Brain Res 921:165-172.
78. Wentzel PR, De Zeeuw CI, Holstege JC, Gerrits NM (1993) Colocalization of GABA and glycine in the rabbit oculomotor nucleus. Neurosci Lett 164:25-29.
79. Wood DE, Stein W, Nusbaum MP (2000) Projection neurons with shared cotransmitters elicit different motor patterns from the same neural circuit. J Neurosci 20:8943-8953.