Tonic GABAA conductance bidirectionally controls interneuron firing pattern and synchronization in the CA3 hippocampal network

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages 504-509

  Pavlov, Ivan ^a   Savtchenko, Leonid P ^a,b   Song, Inseon ^b   Koo, Jaeyeon ^b   Pimashkin, Alexey ^c   Rusakov, Dmitri A ^a   Semyanov, Alexey ^b,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c LOBACHEVSKY STATE UNIVERSITY OF NIZHNY NOVGOROD   (Russian Federation)

Author keywords

Extrasynaptic signaling; Oscillations; Tonic conductance

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID; GRAMICIDIN;

ANIMAL CELL; ARTICLE; BRAIN FUNCTION; CELL FUNCTION; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; ELECTROENCEPHALOGRAM; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HIPPOCAMPAL CA3 REGION; INTERNEURON; MOLECULAR DYNAMICS; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SHUNTING; SPIKE; SYNAPSE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BRAIN; CHEMISTRY; CYTOLOGY; EXTRASYNAPTIC SIGNALING; MALE; METABOLISM; NERVE CELL; OSCILLATIONS; OSCILLOMETRY; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PRENATAL DEVELOPMENT; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION; TIME; TONIC CONDUCTANCE;

EXTRASYNAPTIC SIGNALING; OSCILLATIONS; TONIC CONDUCTANCE;

ACTION POTENTIALS; ANIMALS; BRAIN; CA3 REGION, HIPPOCAMPAL; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GRAMICIDIN; INTERNEURONS; MALE; MODELS, BIOLOGICAL; MODELS, NEUROLOGICAL; NEURONS; OSCILLOMETRY; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 84891922354     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1308388110     Document Type: Article

References (28)

1. Mann EO, Paulsen O (2007) Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci 30(7): 343-349.
2. Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8(1): 45-56.
3. Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49(1): 107-117.
4. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven bymetabotropic glutamate receptor activation. Nature 373(6515): 612-615.
5. Semyanov A, Walker MC, Kullmann DM, Silver RA (2004) Tonically active GABA A receptors: Modulating gain and maintaining the tone. Trends Neurosci 27(5): 262-269.
6. Semyanov A, Walker MC, Kullmann DM (2003) GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6(5): 484-490.
7. Bouwman BM, Heesen E, van Rijn CM (2004) The interaction between vigabatrin and diazepam on the electroencephalogram during active behaviour in rats: An isobolic analysis. Eur J Pharmacol 495(2-3): 119-128.
8. Lu CB, Yanagawa Y, Henderson Z (2010) Properties of gamma frequency oscillatory activity induced in hippocampal slices from the adult GAD67-GFP (Deltaneo) mouse. Brain Res 1323: 65-73.
9. Héja L, et al. (2012) Astrocytes convert network excitation to tonic inhibition of neurons. BMC Biol 10:26.
10. Mann EO, Mody I (2010) Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat Neurosci 13(2): 205-212.
11. Farrant M, Kaila K (2007) The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 160: 59-87.
12. Michelson HB, Wong RK (1991) Excitatory synaptic responses mediated by GABAA receptors in the hippocampus. Science 253(5026): 1420-1423.
13. Verheugen JA, Fricker D, Miles R (1999) Noninvasive measurements of the membrane potential and GABAergic action in hippocampal interneurons. J Neurosci 19(7): 2546-2555.
14. Song I, Savtchenko L, Semyanov A (2011) Tonic excitation or inhibition is set by GABA (A) conductance in hippocampal interneurons. Nat Commun 2:376.
15. Sauer JF, Strüber M, Bartos M (2012) Interneurons provide circuit-specific depolarization and hyperpolarization. J Neurosci 32(12): 4224-4229.
16. Zhang SJ, Jackson MB (1995) GABAA receptor activation and the excitability of nerve terminals in the rat posterior pituitary. J Physiol 483(Pt 3): 583-595.
17. Banke TG, McBain CJ (2006) GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 26(45): 11720-11725.
18. Fano U (1947) Ionization yield of radiations. 2. The fluctuations of the number of ions. Phys Rev 72(1): 26-29.
19. Wang XJ, Buzsáki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16(20): 6402-6413.
20. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394(6689): 186-189.
21. Hopfield JJ (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376(6535): 33-36.
22. Ascoli GA, Gasparini S, Medinilla V, Migliore M (2010) Local control of postinhibitory rebound spiking in CA1 pyramidal neuron dendrites. J Neurosci 30(18): 6434-6442.
23. Manseau F, Goutagny R, Danik M, Williams S (2008) The hippocamposeptal pathway generates rhythmic firing of GABAergic neurons in the medial septum and diagonal bands: an investigation using a complete septohippocampal preparation in vitro. J Neurosci 28(15): 4096-4107.
24. Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann DM (2012) Oscillatory dynamics in the hippocampus support dentate gyrus-CA3 coupling. Nat Neurosci 15(5): 763-768.
25. Song I, et al. (2013) Different transporter systems regulate extracellular GABA from vesicular and non-vesicular sources. Front Cell Neurosci 7:23.
26. Kopell N, Borgers C, Pervouchine D, Malerba P, Tort ABL (2010) Gamma and theta rhythms in biophysical models of hippocampal circuits. Hippocampal Microcircuits: A Computational Modeller's Resource Book, eds Cutsuridis V, Graham BP, Cobb S, Vida I (Springer, Berlin), Chap 15.
27. 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(48): 15341-15350.
28. Zheng K, Scimemi A, Rusakov DA (2008) Receptor actions of synaptically released glutamate: The role of transporters on the scale from nanometers to microns. Biophys J 95(10): 4584-4596.