Increase of GABAA receptor-mediated tonic inhibition in DG c(11)

474Z.Mtchedlishvilietal./NeurobiologyofDisease38(2010)464–475

Das,P.,Bell-Horner,C.L.,Huang,R.Q.,Raut,A.,Gonzales,E.B.,Chen,Z.L.,Covey,D.F.,Dillon,

G.H.,2004.InhibitionoftypeAGABAreceptorsbyL-typecalciumchannelblockers.Neuroscience124,195–206.

Dawson,G.R.,Maubach,K.A.,Collinson,N.,Cobain,M.,Everitt,B.J.,MacLeod,A.M.,Choudhury,

H.I.,McDonald,L.M.,Pillai,G.,Rycroft,W.,Smith,A.J.,Sternfeld,F.,Tattersall,F.D.,Wafford,K.A.,Reynolds,D.S.,Seabrook,G.R.,Atack,J.R.,2006.Aninverseagonistselectiveforalpha5subunit-containingGABAAreceptorsenhancescognition.J.Pharmacol.Exp.Ther.316,1335–1345.

DeRidder,M.N.,Simon,M.J.,Siman,R.,Auberson,Y.P.,Raghupathi,R.,Meaney,D.F.,2006.

Traumaticmechanicalinjurytothehippocampusinvitrocausesregionalcaspase-3andcalpainactivationthatisin uencedbyNMDAreceptorsubunitcomposition.Neurobiol.Dis.22,165–176.

Dinocourt,C.,Gallagher,S.E.,Thompson,S.M.,2006.Injury-inducedaxonalsproutinginthe

hippocampusisinitiatedbyactivationoftrkBreceptors.Eur.J.Neurosci.24,1857–1866.Dixon,C.E.,Lighthall,J.W.,Anderson,T.E.,1988.Physiologic,histopathologic,and

cineradiographiccharacterizationofanew uid-percussionmodelofexperimentalbraininjuryintherat.J.Neurotrauma5,91–104.

Dixon,C.E.,Clifton,G.L.,Lighthall,J.W.,Yaghmai,A.A.,Hayes,R.L.,1991.Acontrolledcortical

impactmodeloftraumaticbraininjuryintherat.J.Neurosci.Methods39,253–262.Edwards,F.A.,Konnerth,A.,Sakmann,B.,1990.Quantalanalysisofinhibitorysynaptic

transmissioninthedentategyrusofrathippocampalslices:apatch-clampstudy.J.Physiol.430,213–249.

Elmer,E.,Kokaia,Z.,Kokaia,M.,Carnahan,J.,Nawa,H.,Lindvall,O.,1998.Dynamicchanges

ofbrain-derivedneurotrophicfactorproteinlevelsintheratforebrainaftersingleandrecurringkindling-inducedseizures.Neuroscience83,351–362.

Engel,A.K.,Singer,W.,2001.Temporalbindingandtheneuralcorrelatesofsensory

awareness.TrendsCogn.Sci.5,16–25.

Ernfors,P.,Bengzon,J.,Kokaia,Z.,Persson,H.,Lindvall,O.,1991.Increasedlevelsof

messengerRNAsforneurotrophicfactorsinthebrainduringkindlingepileptogenesis.Neuron7,165–176.

Essrich,C.,Lorez,M.,Benson,J.,Fritschy,J.M.,Luscher,B.,1998.Postsynapticclusteringof

majorGABAAreceptorsubtypesrequirestheγ2subunitandgephyrin.Nat.Neurosci.1,563–571.

Eugène,E.,Depienne,C.,Baulac,S.,Baulac,M.,Fritschy,J.M.,LeGuern,E.,Miles,R.,

Poncer,J.C.,2007.GABA(A)receptorgamma2subunitmutationslinkedtohumanepilepticsyndromesdifferentiallyaffectphasicandtonicinhibition.J.Neurosci.27,14108–14116.

Falkenberg,T.,Mohammed,A.K.,Henriksson,B.,Persson,H.,Winblad,B.,Lindefors,N.,

1992.Increasedexpressionofbrain-derivedneurotrophicfactormRNAinrathippocampusisassociatedwithimprovedspatialmemoryandenrichedenvironment.Neurosci.Lett.138,153–156.

Feng,H.J.,Mathews,G.C.,Kao,C.,Macdonald,R.L.,2008.AlterationsofGABAA-receptorfunctionandallostericmodulationduringdevelopmentofstatusepilepticus.J.Neurophysiol.99,1285–1293.

Gao,L.,Green eld,L.J.,2005.ActivationofproteinkinaseCreducesbenzodiazepine

potencyatGABAAreceptorsinNT2-Nneurons.Neuropharmacology48,333–342.GibbsIII,J.W.,Sombati,S.,DeLorenzo,R.J.,Coulter,D.A.,1997.Physiologicaland

pharmacologicalalterationsinpostsynapticGABA(A)receptorfunctioninahippocam-palculturemodelofchronicspontaneousseizures.J.Neurophysiol.77,2139–2152.Glykys,J.,Mann,E.O.,Mody,I.,2008.WhichGABA(A)receptorsubunitsarenecessaryfor

tonicinhibitioninthehippocampus?J.Neurosci.28,1421–1426.

Golarai,G.,Greenwood,A.C.,Feeney,D.M.,Connor,J.A.,2001.Physiologicalandstructural

evidenceforhippocampalinvolvementinpersistentseizuresusceptibilityaftertraumaticbraininjury.J.Neurosci.21,8523–8537.

Goldschen-Ohm,M.P.,Wagner,D.A.,Petrou,S.,Jones,M.V.,2010.Anepilepsy-related

regionintheGABA(A)receptormediateslong-distanceeffectsonGABAandbenzodiazepinebindingsites.Mol.Pharmacol.77,35–45.

Goodkin,H.P.,Yeh,J.L.,Kapur,J.,2005.Statusepilepticusincreasestheintracellular

accumulationofGABAAreceptors.J.Neurosci.25,5511–5520.

Goodkin,H.P.,Joshi,S.,Mtchedlishvili,Z.,Brar,J.,Kapur,J.,2008.Subunit-speci ctraf cking

ofGABA(A)receptorsduringstatusepilepticus.J.Neurosci.28,2527–2538.

Hájos,N.,Nusser,Z.,Rancz,E.A.,Freund,T.F.,Mody,I.,2000.Celltype-andsynapse-speci c

variabilityinsynapticGABAAreceptoroccupancy.Eur.J.Neurosci.12,810–818.

Halasy,K.,Somogyi,P.,1993.SubdivisionsinthemultipleGABAergicinnervationof

granulecellsinthedentategyrusoftherathippocampus.Eur.J.Neurosci.5,411–429.Hall,S.,Bornstein,R.A.,1991.Therelationshipbetweenintelligenceandmemory

followingminorormildclosedheadinjury:greaterimpairmentinmemorythanintelligence.J.Neurosurg.75,378–381.

Hamann,M.,Rossi,D.J.,Attwell,D.,2002.Tonicandspilloverinhibitionofgranulecells

controlinformation owthroughcerebellarcortex.Neuron33,625–633.

Hardingham,N.R.,Larkman,A.U.,1998.Rapidreport:thereliabilityofexcitatorysynaptic

transmissioninslicesofratvisualcortexinvitroistemperaturedependent.J.Physiol.507,249–256.

Heinemann,U.,Beck,H.,Dreier,J.P.,Ficker,E.,Stabel,J.,Zhang,C.L.,1992.Thedentate

gyrusasaregulatedgateforthepropagationofepileptiformactivity.EpilepsyRes.7,273–280.

Hicks,R.R.,Numan,S.,Dhillon,H.S.,Prasad,M.R.,Seroogy,K.B.,1997.AlterationsinBDNF

andNT-3mRNAsinrathippocampusafterexperimentalbraintrauma.BrainRes.48,401–406.

Hübner,C.A.,Stein,V.,Hermans-Borgmeyer,I.,Meyer,T.,Ballanyi,K.,Jentsch,T.J.,2001.

DisruptionofKCC2revealsanessentialroleofK–Clcotransportalreadyinearlysynapticinhibition.Neuron30,515–524.

Hunt,R.F.,Scheff,S.W.,Smith,B.N.,2009.Posttraumaticepilepsyaftercontrolledcortical

impactinjuryinmice.Exp.Neurol.215,243–252.

Johansson,I.M.,Birzniece,V.,Lindblad,C.,Olsson,T.,Backstrom,T.,2002.Allopregna-noloneinhibitslearningintheMorriswatermaze.BrainRes.934,125–131.

Joshi,S.,Kapur,J.,2009.SlowintracellularaccumulationofGABA(A)receptordeltasubunit

ismodulatedbybrain-derivedneurotrophicfactor.Neuroscience164,507–519.

Kaneda,M.,Farrant,M.,Cull-Candy,S.G.,1995.Whole-cellandsingle-channelcurrents

activatedbyGABAandglycineingranulecellsoftheratcerebellum.J.Physiol.485,419–435.

Kant,G.J.,Wylie,R.M.,Vasilakis,A.A.,Ghosh,S.,1996.Effectsoftriazolamanddiazepamon

learningandmemoryasassessedusingawatermaze.Pharmacol.Biochem.Behav.53,317–322.

Kapur,J.,Macdonald,R.L.,1997.Rapidseizure-inducedreductionofbenzodiazepineand

Zn2+sensitivityofhippocampaldentategranulecellGABAAreceptors.J.Neurosci.17,7532–7540.

Kharlamov,E.A.,Jukkola,P.I.,Schmitt,K.L.,Kelly,K.M.,2003.Electrobehavioralcharacter-isticsofepilepticratsfollowingphotothromboticbraininfarction.EpilepsyRes.56,185–203.

Kittler,J.T.,Moss,S.J.,2003.ModulationofGABAAreceptoractivitybyphosphorylationand

receptortraf cking:implicationsfortheef cacyofsynapticinhibition.Curr.Opin.Neurobiol.13,341–347.

Kneussel,M.,Betz,H.,2000.Receptors,gephyrinandgephyrin-associatedproteins:

novelinsightsintotheassemblyofinhibitorypostsynapticmembranespecializa-tions.J.Physiol.525,1–9.

Kobori,N.,Clifton,G.L.,Dash,P.K.,2006.Enhancedcatecholaminesynthesisinthe

prefrontalcortexaftertraumaticbraininjury:implicationsforprefrontaldysfunction.J.Neurotrauma23,1094–1102.

Korpi,E.R.,Luddens,H.,1997.FurosemideinteractionswithbrainGABA(A)receptors.

Br.J.Pharmacol.120,741–748.

Kozlov,A.S.,Angulo,M.C.,Audinat,E.,Charpak,S.,2006.Targetcell-speci cmodulationof

neuronalactivitybyastrocytes.Proc.Natl.Acad.Sci.U.S.A.27,10058–10063.

Krazem,A.,Borde,N.,Beracochea,D.,2001.Effectsofdiazepamandbeta-CCMonworking

memoryinmice:relationshipswithemotionalreactivity.Pharmacol.Biochem.Behav.68,235–244.

Kushmerick,C.,Renden,R.,vonGersdorff,H.,2006.Physiologicaltemperaturesreducethe

rateofvesiclepooldepletionandshort-termdepressionviaanaccelerationofvesiclerecruitment.J.Neurosci.26,1366–1377.

Levin,H.S.,Grossman,R.G.,Rose,J.E.,Teasdale,G.,1979.Long-termneuropsychological

outcomeofclosedheadinjury.J.Neurosurg.50,412–422.

Liu,Q.Y.,Schaffner,A.E.,Chang,Y.H.,Maric,D.,Barker,J.L.,2000.Persistentactivationof

GABA(A)receptor/Cl( )channelsbyastrocyte-derivedGABAinculturedembryonicrathippocampalneurons.J.Neurophysiol.84,1392–1403.

Llinas,R.,Ribary,U.,2001.Consciousnessandthebrain.Thethalamocorticaldialoguein

healthanddisease.Ann.N.Y.Acad.Sci.929,166–175.

Mangan,P.S.,Sun,C.,Carpenter,M.,Goodkin,H.P.,Sieghart,W.,Kapur,J.,2005.Cultured

hippocampalpyramidalneuronsexpresstwokindsofGABAAreceptors.Mol.Pharmacol.67,775–788.

Mann,E.O.,Mody,I.,2009.Controlofhippocampalgammaoscillationfrequencyby

tonicinhibitionandexcitationofinterneurons.Nat.Neurosci.13,205–212.

Maubach,K.,2003.GABA(A)receptorsubtypeselectivecognitionenhancers.Curr.Drug

TargetsCNSNeurol.Disord.2,233–239.

Mayo,W.,Dellu,F.,Cherkaoui,J.,Chapouthier,G.,Dodd,R.H.,Le,M.M.,Simon,H.,1992.

Cognitiveenhancingpropertiesofbeta-CCMinfusedintothenucleusbasalismagnocellularisoftherat.BrainRes.589,109–114.

Mayo,W.,Dellu,F.,Robel,P.,Cherkaoui,J.,Le,M.M.,Baulieu,E.E.,Simon,H.,1993.Infusion

ofneurosteroidsintothenucleusbasalismagnocellularisaffectscognitiveprocessesintherat.BrainRes.607,324–328.

Merlio,J.P.,Ernfors,P.,Kokaia,Z.,Middlemas,D.S.,Bengzon,J.,Kokaia,M.,Smith,M.L.,

Siesjo,B.K.,Hunter,T.,Lindvall,O.,Persson,H.,1993.IncreasedproductionoftheTrkBproteintyrosinekinasereceptorafterbraininsults.Neuron10,151–164.

Micheva,K.D.,Smith,S.J.,2005.Strongeffectsofsubphysiologicaltemperatureonthe

functionandplasticityofmammalianpresynapticterminals.J.Neurosci.25,7481–7488.Miles,R.,Tóth,K.,Gulyás,A.I.,Hájos,N.,Freund,T.F.,1996.Differencesbetweensomatic

anddendriticinhibitioninthehippocampus.Neuron16,815–823.

Mody,I.,Pearce,R.A.,2004.DiversityofinhibitoryneurotransmissionthroughGABA(A)

receptors.TrendsNeurosci.27,569–575.

Mtchedlishvili,Z.,Kapur,J.,2006.High-af nity,slowlydesensitizingGABAAreceptors

mediatetonicinhibitioninhippocampaldentategranulecells.Mol.Pharmacol.69,564–575.

Naylor,D.E.,Liu,H.,Wasterlain,C.G.,2005.Traf ckingofGABA(A)receptors,lossof

inhibition,andamechanismforpharmacoresistanceinstatusepilepticus.J.Neurosci.25,7724–7733.

Nusser,Z.,Mody,I.,2002.Selectivemodulationoftonicandphasicinhibitionsindentate

gyrusgranulecells.J.Neurophysiol.87,2624–2628.

Nusser,Z.,Roberts,J.D.,Baude,A.,Richards,J.G.,Somogyi,P.,1995.Relativedensitiesof

synapticandextrasynapticGABAAreceptorsoncerebellargranulecellsasdeterminedbyaquantitativeimmunogoldmethod.J.Neurosci.15,2948–2960.

Nusser,Z.,Hajos,N.,Somogyi,P.,Mody,I.,1998.IncreasednumberofsynapticGABA(A)

receptorsunderliespotentiationathippocampalinhibitorysynapses.Nature395,172–177.

O'Dell,D.M.,Hamm,R.J.,1995.ChronicpostinjuryadministrationofMDL26,479

(Suritozole),anegativemodulatorattheGABAAreceptor,andcognitiveimpairmentinratsfollowingtraumaticbraininjury.J.Neurosurg.83,878–883.

Otis,T.S.,De,K.Y.,Mody,I.,stingpotentiationofinhibitionisassociatedwithan

increasednumberofgamma-aminobutyricacidtypeAreceptorsactivatedduringminiatureinhibitorypostsynapticcurrents.Proc.Natl.Acad.Sci.U.S.A.91,7698–7702.Payne,H.L.,Donoghue,P.S.,Connelly,W.M.,Hinterreiter,S.,Tiwari,P.,Ives,J.H.,

Hann,V.,Sieghart,W.,Lees,G.,Thompson,C.L.,2006.AberrantGABA(A)receptorexpressioninthedentategyrusoftheepilepticmutantmousestargazer.J.Neurosci.26,8600–8608.