Presynaptic but not postsynaptic GABA signaling at Unitary mossy Fiber Synapses

Journal of Neuroscience

Volumn 32, Issue 34, 2012, Pages 11835-11840

  Cabezas, Carolina ^a,b,c   Irinopoulou, Theano ^a,b   Gauvain, Grégory ^a,b   Poncer, Jean Christophe ^a,b  

^a INSTITUT DU FER À MOULIN   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; DOUBLECORTIN; GLUTAMATE DECARBOXYLASE; NEURON SPECIFIC NUCLEAR PROTEIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; EXCITABILITY; GRANULE CELL; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; MALE; MOSSY FIBER; MOUSE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; BEE VENOMS; CARRIER PROTEINS; EXCITATORY POSTSYNAPTIC POTENTIALS; FUNCTIONAL LATERALITY; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HOMEODOMAIN PROTEINS; IMAGING, THREE-DIMENSIONAL; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOSSY FIBERS, HIPPOCAMPAL; NEURONS; PHOSPHINIC ACIDS; POTASSIUM CHANNEL BLOCKERS; PRESYNAPTIC TERMINALS; PROPANOLAMINES; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84865204711     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5543-11.2012     Document Type: Article

References (35)

1. Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365-381.
2. Bergersen L, Ruiz A, Bjaalie JG, Kullmann DM, Gundersen V (2003) GABA and GABAA receptors at hippocampal mossy fibre synapses. Eur J Neurosci 18:931-941.
3. Bouzigues C, Morel M, Triller A, Dahan M (2007) Asymmetric redistribution of GABA receptors during GABA gradient sensing by nerve growth cones analyzed by single quantum dot imaging. Proc Natl Acad Sci U S A 104:11251-11256.
4. Bucher D, Goaillard JM (2011) Beyond faithful conduction: short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Prog Neurobiol 94:307-346.
5. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611.
6. Faulkner RL, Jang MH, Liu XB, Duan X, Sailor KA, Kim JY, Ge S, Jones EG, Ming GL, Song H, Cheng HJ (2008) Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain. Proc Natl Acad Sci U S A 105:14157-14162.
7. Gómez-Lira G, Trillo E, Ramírez M, Asai M, Sitges M, Gutiérrez R (2002) The expression of GABA in mossy fiber synaptosomes coincides with the seizure-induced expression of GABAergic transmission in the mossy fiber synapse. Exp Neurol 177:276-283.
8. Gutiérrez R, Romo-Parra H, Maqueda J, Vivar C, Ramìrez M, Morales MA, Lamas M (2003) Plasticity of the GABAergic phenotype of the "glutamatergic" granule cells of the rat dentate gyrus. J Neurosci 23:5594-5598.
9. Houser CR (2007) Interneurons of the dentate gyrus: an overview of cell types, terminal fields and neurochemical identity. Prog Brain Res 163:217-232.
10. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol 472:615-663.
11. Kulik A, Vida I, Fukazawa Y, Guetg N, Kasugai Y, Marker CL, Rigato F, Bettler B, Wickman K, Frotscher M, Shigemoto R (2006) Compartmentdependent colocalization of Kir3.2-containing K+channels and GABAB receptors in hippocampal pyramidal cells. J Neurosci 26:4289-4297.
12. Ladera C, del Carmen Godino M, José Cabañero M, Torres M, Watanabe M, Luján R, Sánchez-Prieto J (2008) Pre-synaptic GABA receptors inhibit glutamate release through GIRK channels in rat cerebral cortex. J Neurochem 107:1506-1517.
13. Lübke J, Frotscher M, Spruston N (1998) Specialized electrophysiological properties of anatomically identified neurons in the hilar region of the rat fascia dentata. J Neurophysiol 79:1518-1534.
14. Lujan R, Maylie J, Adelman JP (2009) New sites of action for GIRK and SK channels. Nat Rev 10:475-480.
15. Lüscher C, Jan LY, Stoffel M, Malenka RC, Nicoll RA (1997) G proteincoupled inwardly rectifying K + channels (GIRKs) mediate postsynaptic but not presynaptic transmitter actions in hippocampal neurons. Neuron 19:687-695.
16. McBain CJ (2008) Differential mechanisms of transmission and plasticity at mossy fiber synapses. Prog Brain Res 169:225-240.
17. Michaeli A, Yaka R (2010) Dopamine inhibits GABA(A) currents in ventral tegmental area dopamine neurons via activation of presynaptic G-protein coupled inwardly-rectifying potassium channels. Neuroscience 165:1159-1169.
18. Mori M, Abegg MH, Gähwiler BH, Gerber U (2004) A frequencydependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431:453-456.
19. Overstreet-Wadiche LS, Bensen AL, Westbrook GL (2006) Delayed development of adult-generated granule cells in dentate gyrus. J Neurosci 26:2326-2334.
20. Poncer JC, McKinney RA, Gahwiler BH, Thompson SM (2000) Differential control of GABA release at synapses from distinct interneurons in rat hippocampus. J Physiol 528:123-130.
21. Ruiz A, Fabian-Fine R, Scott R, Walker MC, Rusakov DA, Kullmann DM (2003) GABAA receptors at hippocampal mossy fibers. Neuron 39:961-973.
22. Ruiz A, Campanac E, Scott RS, Rusakov DA, Kullmann DM (2010) Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat Neurosci 13:431-438.
23. Safiulina VF, Fattorini G, Conti F, Cherubini E (2006) GABAergic signaling at mossy fiber synapses in neonatal rat hippocampus. J Neurosci 26:597-608.
24. Sandler R, Smith AD (1991) Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 303:177-192.
25. Scheuber A, Miles R, Poncer JC (2004) Presynaptic Cav2.1 and Cav2.2 differentially influence release dynamics at hippocampal excitatory synapses. J Neurosci 24:10402-10409.
26. Sloviter RS, Dichter MA, Rachinsky TL, Dean E, Goodman JH, Sollas AL, Martin DL (1996) Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 373:593-618.
27. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
28. Toni N, Laplagne DA, Zhao C, Lombardi G, Ribak CE, Gage FH, Schinder AF (2008) Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci 11:901-907.
29. Uchigashima M, Fukaya M, Watanabe M, Kamiya H (2007) Evidence against GABA release from glutamatergic mossy fiber terminals in the developing hippocampus. J Neurosci 27:8088-8100.
30. Vogt KE, Nicoll RA (1999) Glutamate and gamma-aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus. Proc Natl Acad Sci U S A 96:1118-1122.
31. 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.
32. Wu Y, Wang W, Díez-Sampedro A, Richerson GB (2007) Nonvesicular inhibitory neurotransmission via reversal of the GABA transporter GAT-1. Neuron 56:851- 865.
33. Xiang Y, Li Y, Zhang Z, Cui K, Wang S, Yuan XB, Wu CP, Poo MM, Duan S (2002) Nerve growth cone guidance mediated by G protein-coupled receptors. Nat Neurosci 5:843-848.
34. Zander JF, Münster-Wandowski A, Brunk I, Pahner I, Gómez-Lira G, Heinemann U, Gutiérrez R, Laube G, Ahnert-Hilger G (2010) Synaptic and vesicular coexistence of VGLUT and VGAT in selected excitatory and inhibitory synapses. J Neurosci 30:7634-7645.
35. Zhao S, Zhou Y, Gross J, Miao P, Qiu L, Wang D, Chen Q, Feng G (2010) Fluorescent labeling of newborn dentate granule cells in GAD67-GFP transgenic mice: a genetic tool for the study of adult neurogenesis. PloS One 5:e12506.