Postsynaptic GABAB receptors enhance extrasynaptic GABAA receptor function in dentate gyrus granule cells

Journal of Neuroscience

Volumn 33, Issue 9, 2013, Pages 3738-3743

  Tao, Wucheng ^b   Higgs, Matthew H ^a,b   Spain, William J ^a,b   Ransom, Christopher B ^a,b  

^a VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4, 4 DIPHENYL 3 BUTENYL) NIPECOTIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; BACLOFEN; BENZYL [3 [[1 (3, 4 DICHLOROPHENYL) ETHYL] AMINO] 2 HYDROXYPROPYL] PHOSPHINIC ACID; BICUCULLINE METHIODIDE; GABOXADOL; POSTSYNAPTIC RECEPTOR; UNCLASSIFIED DRUG; CONCANAMYCIN A; DRUG DERIVATIVE; ENZYME INHIBITOR; GABAERGIC RECEPTOR AFFECTING AGENT; GUANOSINE 5' O (2 THIODIPHOSPHATE); GUANOSINE 5'-O-(2-THIODIPHOSPHATE); GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MACROLIDE; NUCLEOTIDE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ELECTROPHYSIOLOGY; GABAERGIC TRANSMISSION; GRANULE CELL; HIPPOCAMPAL CA1 REGION; INHIBITORY POSTSYNAPTIC POTENTIAL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PYRAMIDAL NERVE CELL; RAT; SPIKE WAVE; SYNAPSE VESICLE; SYNAPTIC POTENTIAL; ANIMAL; BIOPHYSICS; CYTOLOGY; DRUG EFFECT; DRUG INTERACTION; ELECTROSTIMULATION; FEMALE; IN VITRO STUDY; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SYNAPSE;

ANIMALS; BIOPHYSICS; DENTATE GYRUS; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; FEMALE; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MACROLIDES; MALE; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; THIONUCLEOTIDES;

MLCS; MLOWN;

EID: 84874599832     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4829-12.2013     Document Type: Article

References (36)

1. Allen NJ, Rossi DJ, Attwell D (2004) Sequential release of GABA by exocytosis and reversed uptake leads to neuronal swelling in simulated ischemia of hippocampal slices. J Neurosci 24:3837-3849. CrossRef Medline
2. Andrade R (1991) Blockade of neurotransmitter-activated K+ conductance by QX-314 in the rat hippocampus. Eur J Pharmacol 199:259-262. CrossRef Medline
3. Arima-Yoshida F, Watabe AM, Manabe T (2011) The mechanisms of the strong inhibitory modulation of long-term potentiation in the rat dentate gyrus. Eur J Neurosci 33:1637-1646. CrossRef Medline
4. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by α5 subunit-containing gamma-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 101:3662-3667. CrossRef Medline
5. Chadderton P, Margrie TW, Häusser M (2004) Integration of quanta in cerebellar granule cells during sensory processing. Nature 428:856-860. CrossRef Medline
6. Chen C, Regehr WG (2003) Presynaptic modulation of the retinogeniculate synapse. J Neurosci 23:3130-3135. Medline
7. Cope DW, Di Giovanni G, Fyson SJ, Orbán G, Errington AC, Lorincz ML, Gould TM, Carter DA, Crunelli V (2009) Enhanced tonic GABAA inhibition in typical absence epilepsy. Nat Med 15:1392-1398. CrossRef Medline
8. Duguid I, Branco T, London M, Chadderton P, Häusser M (2012) Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J Neurosci 32:11132-11143. CrossRef Medline
9. During MJ, Spencer DD (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341:1607-1610. CrossRef Medline
10. Dutar P, Nicoll RA (1988) Pre-and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1:585-591. CrossRef Medline
11. A receptors. Nat Rev Neurosci 6:215-229. CrossRef Medline
12. A receptor α5 subunit-deficient mice. J Neurophysiol 95:2796-2807. CrossRef Medline
13. A receptors: views from outside the synaptic cleft. Neuron 56:763-770. CrossRef Medline
14. A receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 28:1421-1426. CrossRef Medline
15. Gupta A, Elgammal FS, Proddutur A, Shah S, Santhakumar V (2012) Decrease in tonic inhibition contributes to increase in dentate semilunar granule cell excitability after brain injury. J Neurosci 32:2523-2537. CrossRef Medline
16. Harayama N, Shibuya I, Tanaka K, Kabashima N, Ueta Y, Yamashita H (1998) Inhibition of N-and P/Q-type calcium channels by postsynaptic GABABreceptor activation in rat supraoptic neurones. J Physiol 509:371-383. CrossRef Medline
17. Holter NI, Zylla MM, Zuber N, Bruehl C, Draguhn A (2010) Tonic GABAergic control of mouse dentate granule cells during postnatal development. Eur J Neurosci 32:1300-1309. CrossRef Medline
18. Kulik A, Vida I, Luján R, Haas CA, Lopez-Bendito G, Shigemoto R, Frotscher M (2003) Subcellular localization of metabotropic GABA(B) receptor subunits GABA(B1a/b) and GABA(B2) in the rat hippocampus. J Neurosci 23:11026-11035. Medline
19. Lin HH, Dun NJ (1998) Post-and presynaptic GABA(B) receptor activation in neonatal rat rostral ventrolateral medulla neurons in vitro. Neuroscience 86:211-220. CrossRef Medline
20. A receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8:797-804. CrossRef Medline
21. Martin LJ, Zurek AA, MacDonald JF, Roder JC, Jackson MF, Orser BA (2010) alpha5 GABAA receptor activity sets the threshold for long-term potentiation and constrains hippocampus-dependent memory. J Neurosci 30:5269-5282. CrossRef Medline
22. Meera P, Wallner M, Otis TS (2011) Molecular basis for the high THIP/ gaboxadol sensitivity of extrasynaptic GABAA receptors. J Neurophysiol 106:2057-2064. CrossRef Medline
23. Mortensen M, Ebert B, Wafford K, Smart TG (2010) Distinct activities of GABA agonists at synaptic-and extrasynaptic-type GABAA receptors. J Physiol 588:1251-1268. CrossRef Medline
24. Nathan T, Jensen MS, Lambert JDC (1990) The slow inhibitory postsynaptic potential in rat hippocampal CA1 neurones is blocked by intracellular injection of QX-314. Neurosci Lett 110:309-313. CrossRef Medline
25. Nusser Z, Mody I (2002) Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87:2624-2628. Medline
26. Otis TS, Mody I (1992) Differential activation of GABAA and GABAB receptors by spontaneously released transmitter. J Neurophysiol 67: 227-235. Medline
27. Overstreet LS, Westbrook GL (2001) Paradoxical reduction of synaptic inhibition by vigabatrin. J Neurophysiol 86:596-603. Medline
28. Padgett CL, Slesinger PA (2010) GABAB receptor coupling to G-proteins and ion channels. Adv Pharmacol 58:123-147. CrossRef Medline
29. Pavlov I, Savtchenko LP, Kullmann DM, Semyanov A, Walker MC (2009) Outwardly rectifying tonically active GABAA receptors in pyramidal cells modulate neuronal offset, not gain. J Neurosci 29:15341-15350. CrossRef Medline
30. Ransom CB, Wu Y, Richerson GB (2010) Postdepolarization potentiation of GABAA receptors: a novel mechanism regulating tonic conductance in hippocampal neurons. J Neurosci 30:7672-7684. CrossRef Medline
31. Scanziani M (2000) GABA spillover activates postsynaptic GABA(B) receptors to control rhythmic hippocampal activity. Neuron 25:673-681. CrossRef Medline
32. Scanziani M, Gähwiler BH, Thompson SM (1991) Paroxysmal inhibitory potentials mediated by GABAB receptors in partially disinhibited rat hippocampal slice cultures. J Physiol 444:375-396. Medline
33. Stell BM, Brickley SG, Tang CY, Farrant M, Mody I (2003) Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc Natl Acad Sci U S A 100:14439-14444. CrossRef Medline
34. Wei W, Zhang N, Peng Z, Houser CR, Mody I (2003) Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 23:10650-10661. Medline
35. Wu Y, Wang W, Richerson GB (2003) Vigabatrin induces tonic inhibition via GABA transporter reversal without increasing vesicular GABA release. J Neurophysiol 89:2021-2034. Medline
36. Yamada J, Furukawa T, Ueno S, Yamamoto S, Fukuda A (2007) Molecular basis for the GABAA receptor-mediated tonic inhibition in rat somatosensory cortex. Cereb Cortex 17:1782-1787. CrossRef Medline