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Mechanisms regulating GABAergic inhibitory transmission in the basolateral amygdala: implications for epilepsy and anxiety disorders

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Summary.

The amygdala, a temporal lobe structure that is part of the limbic system, has long been recognized for its central role in emotions and emotional behavior. Pathophysiological alterations in neuronal excitability in the amygdala are characteristic features of certain psychiatric illnesses, such as anxiety disorders and depressive disorders. Furthermore, neuronal excitability in the amygdala, and, in particular, excitability of the basolateral nucleus of the amygdala (BLA) plays a pivotal role in the pathogenesis and symptomatology of temporal lobe epilepsy. Here, we describe two recently discovered mechanisms regulating neuronal excitability in the BLA, by modulating GABAergic inhibitory transmission. One of these mechanisms involves the regulation of GABA release via kainate receptors containing the GluR5 subunit (GluR5KRs). In the rat BLA, GluR5KRs are present on both somatodendritic regions and presynaptic terminals of GABAergic interneurons, and regulate GABA release in an agonist concentration-dependent, bidirectional manner. The relevance of the GluR5KR function to epilepsy is suggested by the findings that GluR5KR agonists can induce epileptic activity, whereas GluR5KR antagonists can prevent it. Further support for an important role of GluR5KRs in epilepsy comes from the findings that antagonism of GluR5KRs is a primary mechanism underlying the antiepileptic properties of the anticonvulsant topiramate. Another mechanism regulating neuronal excitability in the BLA by modulating GABAergic synaptic transmission is the facilitation of GABA release via presynaptic α1A adrenergic receptors. This mechanism may significantly underlie the antiepileptic properties of norepinephrine. Notably, the α1A adrenoceptor-mediated facilitation of GABA release is severely impaired by stress. This stress-induced impairment in the noradrenergic facilitation of GABA release in the BLA may underlie the hyperexcitability of the amygdala in certain stress-related affective disorders, and may explain the stress-induced exacerbation of seizure activity in epileptic patients.

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References

  • HC Abercrombie SM Schaefer CL Larson TR Oakes KA Lindgren JE Holden SB Perlman PA Turski DD Krahn RM Benca RJ Davidson (1998) ArticleTitleMetabolic rate in the right amygdala predicts negative affect in depressed patients Neuroreport 9 3301–3307 Occurrence Handle9831467 Occurrence Handle1:STN:280:DyaK1M%2FkslelsA%3D%3D

    PubMed  CAS  Google Scholar 

  • G Aston-Jones JD Cohen (2005) ArticleTitleAn integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance Annu Rev Neurosci 28 403–450 Occurrence Handle16022602 Occurrence Handle1:CAS:528:DC%2BD2MXosVegtbw%3D

    PubMed  CAS  Google Scholar 

  • CW Berridge BD Waterhouse (2003) ArticleTitleThe locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes Brain Res Rev 42 33–84 Occurrence Handle12668290

    PubMed  Google Scholar 

  • B Bettler J Boulter I Hermans-Borgmeyer A O’Shea-Greenfield ES Deneris C Moll U Borgmeyer M Hollmann S Heinemann (1990) ArticleTitleCloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development Neuron 5 583–595 Occurrence Handle1977421 Occurrence Handle1:CAS:528:DyaK3MXlsFaitro%3D

    PubMed  CAS  Google Scholar 

  • ZA Bortolotto VR Clarke CM Delany MC Parry I Smolders M Vignes KH Ho P Miu BT Brinton R Fantaske A Ogden M Gates PL Ornstein D Lodge D Bleakman GL Collingridge (1999) ArticleTitleKainate receptors are involved in synaptic plasticity Nature 402 297–301 Occurrence Handle10580501 Occurrence Handle1:CAS:528:DyaK1MXnvFShs7Y%3D

    PubMed  CAS  Google Scholar 

  • MF Braga V Aroniadou-Anderjaska H Li (2004a) ArticleTitleThe physiological role of kainate receptors in the amygdala Mol Neurobiol 30 127–141 Occurrence Handle1:CAS:528:DC%2BD2cXptlOku7k%3D

    CAS  Google Scholar 

  • MF Braga V Aroniadou-Anderjaska ST Manion CJ Hough H Li (2004b) ArticleTitleStress impairs alpha(1A) adrenoceptor-mediated noradrenergic facilitation of GABAergic transmission in the basolateral amygdala Neuropsychopharmacology 29 45–58 Occurrence Handle1:CAS:528:DC%2BD3sXhtVSqs7nL

    CAS  Google Scholar 

  • MF Braga V Aroniadou-Anderjaska J Xie H Li (2003) ArticleTitleBidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala J Neurosci 23 442–452 Occurrence Handle12533604 Occurrence Handle1:CAS:528:DC%2BD3sXovV2nug%3D%3D

    PubMed  CAS  Google Scholar 

  • L Cahill JL McGaugh (1998) ArticleTitleMechanisms of emotional arousal and lasting declarative memory Trends Neurosci 21 294–299 Occurrence Handle9683321 Occurrence Handle1:CAS:528:DyaK1cXktl2rur8%3D

    PubMed  CAS  Google Scholar 

  • L Cahill A van Stegeren (2003) ArticleTitleSex-related impairment of memory for emotional events with beta-adrenergic blockade Neurobiol Learn Mem 79 81–88 Occurrence Handle12482682 Occurrence Handle1:CAS:528:DC%2BD38Xps1SjsLs%3D

    PubMed  CAS  Google Scholar 

  • PE Castillo RC Malenka RA Nicoll (1997) ArticleTitleKainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons Nature 388 182–186 Occurrence Handle9217159 Occurrence Handle1:CAS:528:DyaK2sXksFWlsLo%3D

    PubMed  CAS  Google Scholar 

  • F Cendes F Andermann F Dubeau P Gloor A Evans M Jones-Gotman A Olivier E Andermann Y Robitaille I Lopes-Cendes (1993a) ArticleTitleEarly childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study Neurology 43 1083–1087 Occurrence Handle1:STN:280:DyaK2c3isVehtQ%3D%3D

    CAS  Google Scholar 

  • F Cendes F Andermann P Gloor A Evans M Jones-Gotman C Watson D Melanson A Olivier T Peters I Lopes-Cendes (1993b) ArticleTitleMRI volumetric measurement of amygdala and hippocampus in temporal lobe epilepsy Neurology 43 719–725 Occurrence Handle1:STN:280:DyaK3s3is1WjtA%3D%3D

    CAS  Google Scholar 

  • D Chalothorn DF McCune SE Edelmann ML Garcia-Cazarin G Tsujimoto MT Piascik (2002) ArticleTitleDifferences in the cellular localization and agonist-mediated internalization properties of the alpha(1)-adrenoceptor subtypes Mol Pharmacol 61 1008–1016 Occurrence Handle11961118 Occurrence Handle1:CAS:528:DC%2BD38XjtlGltbs%3D

    PubMed  CAS  Google Scholar 

  • CH Chen B Lennox R Jacob A Calder V Lupson R Bisbrown-Chippendale J Suckling E Bullmore (2005) ArticleTitleExplicit and implicit facial affect recognition in manic and depressed states of bipolar disorder: a functional magnetic resonance imaging study Biol Psychiatry 59 31–39 Occurrence Handle16112653

    PubMed  Google Scholar 

  • R Chittajallu SP Braithwaite VR Clarke JM Henley (1999) ArticleTitleKainate receptors: subunits, synaptic localization and function Trends Pharmacol Sci 20 26–35 Occurrence Handle10101959 Occurrence Handle1:CAS:528:DyaK1MXks1amsb0%3D

    PubMed  CAS  Google Scholar 

  • R Chittajallu M Vignes KK Dev JM Barnes GL Collingridge JM Henley (1996) ArticleTitleRegulation of glutamate release by presynaptic kainate receptors in the hippocampus Nature 379 78–81 Occurrence Handle8538745 Occurrence Handle1:CAS:528:DyaK28XivVKgtw%3D%3D

    PubMed  CAS  Google Scholar 

  • VR Clarke BA Ballyk KH Hoo A Mandelzys A Pellizzari CP Bath J Thomas EF Sharpe CH Davies PL Ornstein DD Schoepp RK Kamboj GL Collingridge D Lodge D Bleakman (1997) ArticleTitleA hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission Nature 389 599–603 Occurrence Handle9335499 Occurrence Handle1:CAS:528:DyaK2sXmslWgu78%3D

    PubMed  CAS  Google Scholar 

  • EC Clayton CL Williams (2000) ArticleTitleAdrenergic activation of the nucleus tractus solitarius potentiates amygdala norepinephrine release and enhances retention performance in emotionally arousing and spatial memory tasks Behav Brain Res 112 151–158 Occurrence Handle10862946 Occurrence Handle1:CAS:528:DC%2BD3cXktFCgsbk%3D

    PubMed  CAS  Google Scholar 

  • A Contractor G Swanson SF Heinemann (2001) ArticleTitleKainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus Neuron 29 209–216 Occurrence Handle11182092 Occurrence Handle1:CAS:528:DC%2BD3MXisleisb8%3D

    PubMed  CAS  Google Scholar 

  • ME Corcoran (1988) ArticleTitleCharacteristics of accelerated kindling after depletion of noradrenaline in adult rats Neuropharmacology 27 1081–1084 Occurrence Handle3148871 Occurrence Handle1:CAS:528:DyaL1MXhsVak

    PubMed  CAS  Google Scholar 

  • ME Corcoran ST Mason (1980) ArticleTitleRole of forebrain catecholamines in amygdaloid kindling Brain Res 190 473–484 Occurrence Handle7370800 Occurrence Handle1:CAS:528:DyaL3cXktVGmsr4%3D

    PubMed  CAS  Google Scholar 

  • R Cossart M Esclapez JC Hirsch C Bernard Y Ben-Ari (1998) ArticleTitleGluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells Nat Neurosci 1 470–478 Occurrence Handle10196544 Occurrence Handle1:CAS:528:DyaK1cXmvF2kt70%3D

    PubMed  CAS  Google Scholar 

  • V Crunelli L Cervo R Samanin (1981) Evidence for a preferential role of central noradrenergic neurons in electrically induced convulsions and activity of various anticonvulsants in the rat PR Morselli KG Lloyd (Eds) Neurotransmitters, seizures, and epilepsy Raven Press New York 195–202

    Google Scholar 

  • RA Cunha MD Constantino JA Ribeiro (1997) ArticleTitleInhibition of [3H] gamma-aminobutyric acid release by kainate receptor activation in rat hippocampal synaptosomes Eur J Pharmacol 323 167–172 Occurrence Handle9128835 Occurrence Handle1:CAS:528:DyaK2sXitVKkt78%3D

    PubMed  CAS  Google Scholar 

  • M Davis (1992) ArticleTitleThe role of the amygdala in fear and anxiety Annu Rev Neurosci 15 353–375 Occurrence Handle1575447 Occurrence Handle1:STN:280:DyaK383ks1Cmsw%3D%3D

    PubMed  CAS  Google Scholar 

  • M Davis (1994) ArticleTitleThe role of the amygdala in emotional learning Int Rev Neurobiol 36 225–266 Occurrence Handle7822117 Occurrence Handle1:CAS:528:DyaK2MXhvFyisbc%3D Occurrence Handle10.1016/S0074-7742(08)60305-0

    Article  PubMed  CAS  Google Scholar 

  • F DeBock J Kurz SC Azad CG Parsons G Hapfelmeier W Zieglgansberger G Rammes (2003) ArticleTitleAlpha2-adrenoreceptor activation inhibits LTP and LTD in the basolateral amygdala: involvement of Gi/o-protein-mediated modulation of Ca2+-channels and inwardly rectifying K+-channels in LTD Eur J Neurosci 17 1411–1424 Occurrence Handle12713644 Occurrence Handle1:STN:280:DC%2BD3s3islCgsA%3D%3D

    PubMed  CAS  Google Scholar 

  • Dewar S, Passaro E, Fried I, Engel J Jr (1996) Intracranial electrode monitoring for seizure localization: indications, methods and the prevention of complications. J Neurosci Nurs 28: 280–284, 289–292

    Google Scholar 

  • WC Drevets (1999) ArticleTitlePrefrontal cortical-amygdalar metabolism in major depression Ann NY Acad Sci 877 614–637 Occurrence Handle10415674 Occurrence Handle1:STN:280:DyaK1MzksVWlsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • J Egebjerg SF Heinemann (1993) ArticleTitleCa2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6 Proc Natl Acad Sci USA 90 755–759 Occurrence Handle7678465 Occurrence Handle1:CAS:528:DyaK3sXhsVSjtr8%3D

    PubMed  CAS  Google Scholar 

  • MS Fanselow GD Gale (2003) ArticleTitleThe amygdala, fear, and memory Ann NY Acad Sci 985 125–134 Occurrence Handle12724154 Occurrence Handle10.1111/j.1749-6632.2003.tb07077.x

    Article  PubMed  Google Scholar 

  • B Ferry B Roozendaal JL McGaugh (1999) ArticleTitleRole of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala Biol Psychiatry 46 1140–1152 Occurrence Handle10560021 Occurrence Handle1:CAS:528:DyaK1MXotVOktr4%3D

    PubMed  CAS  Google Scholar 

  • MM Frucht M Quigg C Schwaner NB Fountain (2000) ArticleTitleDistribution of seizure precipitants among epilepsy syndromes Epilepsia 41 1534–1539 Occurrence Handle11114210 Occurrence Handle1:STN:280:DC%2BD3M7hs1SntA%3D%3D

    PubMed  CAS  Google Scholar 

  • K Fuxe A Harfstrand LF Agnati ZY Yu A Cintra AC Wikstrom S Okret E Cantoni JA Gustafsson (1985) ArticleTitleImmunocytochemical studies on the localization of glucocorticoid receptor immunoreactive nerve cells in the lower brain stem and spinal cord of the male rat using a monoclonal antibody against rat liver glucocorticoid receptor Neurosci Lett 60 1–6 Occurrence Handle3903555 Occurrence Handle1:CAS:528:DyaL2MXlvFSiu70%3D

    PubMed  CAS  Google Scholar 

  • R Galvez MH Mesches JL McGaugh (1996) ArticleTitleNorepinephrine release in the amygdala in response to footshock stimulation Neurobiol Learn Mem 66 253–257 Occurrence Handle8946419 Occurrence Handle1:CAS:528:DyaK2sXosFyq

    PubMed  CAS  Google Scholar 

  • FS Giorgi C Pizzanelli F Biagioni L Murri F Fornai (2004) ArticleTitleThe role of norepinephrine in epilepsy: from the bench to the bedside Neurosci Biobehav Rev 28 507–524 Occurrence Handle15465138 Occurrence Handle1:CAS:528:DC%2BD2cXotF2gt7c%3D

    PubMed  CAS  Google Scholar 

  • P Gloor (1992) Role of the amygdala in temporal lobe epilepsy JP Aggleton (Eds) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction Wiley-Liss New York 505–538

    Google Scholar 

  • GV Goddard (1967) ArticleTitleDevelopment of epileptic seizures through brain stimulation at low intensity Nature 214 1020–1021 Occurrence Handle6055396 Occurrence Handle1:STN:280:DyaF1c%2Fhs1aitg%3D%3D

    PubMed  CAS  Google Scholar 

  • LE Goldstein AM Rasmusson BS Bunney RH Roth (1996) ArticleTitleRole of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat J Neurosci 16 4787–4798 Occurrence Handle8764665 Occurrence Handle1:CAS:528:DyaK28XksFWisr0%3D

    PubMed  CAS  Google Scholar 

  • DS Gryder MA Rogawski (2003) ArticleTitleSelective antagonism of GluR5 kainate-receptor-mediated synaptic currents by topiramate in rat basolateral amygdala neurons J Neurosci 23 7069–7074 Occurrence Handle12904467 Occurrence Handle1:CAS:528:DC%2BD3sXmtlyhsb0%3D

    PubMed  CAS  Google Scholar 

  • Habib KE, Gold PW, Chrousos GP (2001) Neuroendocrinology of stress. Endocrinol Metab Clin North Am 30: 695–728; vii–viii

    Google Scholar 

  • A Herb N Burnashev P Werner B Sakmann W Wisden PH Seeburg (1992) ArticleTitleThe KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits Neuron 8 775–785 Occurrence Handle1373632 Occurrence Handle1:CAS:528:DyaK3sXitVGgtb0%3D

    PubMed  CAS  Google Scholar 

  • JE Huettner (2003) ArticleTitleKainate receptors and synaptic transmission Prog Neurobiol 70 387–407 Occurrence Handle14511698 Occurrence Handle1:CAS:528:DC%2BD3sXnsVWltLw%3D

    PubMed  CAS  Google Scholar 

  • L Jiang J Xu M Nedergaard J Kang (2001) ArticleTitleA kainate receptor increases the efficacy of GABAergic synapses Neuron 30 503–513 Occurrence Handle11395010 Occurrence Handle1:CAS:528:DC%2BD3MXktFeit78%3D

    PubMed  CAS  Google Scholar 

  • M Joels ER de Kloet (1989) ArticleTitleEffects of glucocorticoids and norepinephrine on the excitability in the hippocampus Science 245 1502–1505 Occurrence Handle2781292 Occurrence Handle1:CAS:528:DyaL1MXlvVOrsbw%3D

    PubMed  CAS  Google Scholar 

  • EW Kairiss RJ Racine GK Smith (1984) ArticleTitleThe development of the interictal spike during kindling in the rat Brain Res 322 101–110 Occurrence Handle6518361 Occurrence Handle1:STN:280:DyaL2M%2FpvVKltw%3D%3D

    PubMed  CAS  Google Scholar 

  • RM Kaminski M Banerjee MA Rogawski (2004) ArticleTitleTopiramate selectively protects against seizures induced by ATPA, a GluR5 kainate receptor agonist Neuropharmacology 46 1097–1104 Occurrence Handle15111016 Occurrence Handle1:CAS:528:DC%2BD2cXjsVWgs7c%3D

    PubMed  CAS  Google Scholar 

  • SE Krahl KB Clark DC Smith RA Browning (1998) ArticleTitleLocus coeruleus lesions suppress the seizure-attenuating effects of vagus nerve stimulation Epilepsia 39 709–714 Occurrence Handle9670898 Occurrence Handle1:STN:280:DyaK1czjtl2ksQ%3D%3D

    PubMed  CAS  Google Scholar 

  • SE Lauri ZA Bortolotto D Bleakman PL Ornstein D Lodge JT Isaac GL Collingridge (2001) ArticleTitleA critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP Neuron 32 697–709 Occurrence Handle11719209 Occurrence Handle1:CAS:528:DC%2BD3MXovFOis7c%3D

    PubMed  CAS  Google Scholar 

  • JE LeDoux (1992) ArticleTitleBrain mechanisms of emotion and emotional learning Curr Opin Neurobiol 2 191–197 Occurrence Handle1638153 Occurrence Handle1:STN:280:DyaK38zksF2isA%3D%3D

    PubMed  CAS  Google Scholar 

  • J Lerma (2003) ArticleTitleRoles and rules of kainate receptors in synaptic transmission Nat Rev Neurosci 4 481–495 Occurrence Handle12778120 Occurrence Handle1:CAS:528:DC%2BD3sXktFOgtLc%3D

    PubMed  CAS  Google Scholar 

  • H Li MF Braga V Aroniadou-Anderjaska MA Rogawski (2004) ArticleTitleTopiramate modulates neuronal excitability in basolateral amygdala by selectively inhibiting GluR5 kainate receptors and acting as a positive modulator of GABAa receptors Soc Neurosci 16 732

    Google Scholar 

  • H Li A Chen G Xing ML Wei MA Rogawski (2001) ArticleTitleKainate receptor-mediated heterosynaptic facilitation in the amygdala Nat Neurosci 4 612–620 Occurrence Handle11369942 Occurrence Handle1:CAS:528:DC%2BD3MXktFOqtro%3D

    PubMed  CAS  Google Scholar 

  • H Li MA Rogawski (1998) ArticleTitleGluR5 kainate receptor mediated synaptic transmission in rat basolateral amygdala in vitro Neuropharmacology 37 1279–1286 Occurrence Handle9849665 Occurrence Handle1:CAS:528:DyaK1cXnsl2jtro%3D

    PubMed  CAS  Google Scholar 

  • H Li SR Weiss DM Chuang RM Post MA Rogawski (1998) ArticleTitleBidirectional synaptic plasticity in the rat basolateral amygdala: characterization of an activity-dependent switch sensitive to the presynaptic metabotropic glutamate receptor antagonist 2S-alpha-ethylglutamic acid J Neurosci 18 1662–1670 Occurrence Handle9464991 Occurrence Handle1:CAS:528:DyaK1cXht12jtbk%3D

    PubMed  CAS  Google Scholar 

  • AJ McDonald (1998) ArticleTitleCortical pathways to the mammalian amygdala Prog Neurobiol 55 257–332 Occurrence Handle9643556 Occurrence Handle1:STN:280:DyaK1czgsFOjuw%3D%3D

    PubMed  CAS  Google Scholar 

  • AJ McDonald (2003) ArticleTitleIs there an amygdala and how far does it extend? An anatomical perspective Ann NY Acad Sci 985 1–21 Occurrence Handle12724144 Occurrence Handle10.1111/j.1749-6632.2003.tb07067.x

    Article  PubMed  Google Scholar 

  • JL McGaugh (2002) ArticleTitleMemory consolidation and the amygdala: a systems perspective Trends Neurosci 25 456 Occurrence Handle12183206 Occurrence Handle1:CAS:528:DC%2BD38Xmtleksrg%3D

    PubMed  CAS  Google Scholar 

  • JL McGaugh (2004) ArticleTitleThe amygdala modulates the consolidation of memories of emotionally arousing experiences Annu Rev Neurosci 27 1–28 Occurrence Handle15217324 Occurrence Handle1:CAS:528:DC%2BD2cXmslantrk%3D

    PubMed  CAS  Google Scholar 

  • DC McIntyre (1980) ArticleTitleAmygdala kindling in rats: facilitation after local amygdala norepinephrine depletion with 6-hydroxydopamine Exp Neurol 69 395–407 Occurrence Handle7409053 Occurrence Handle1:CAS:528:DyaL3cXltVyjsbc%3D

    PubMed  CAS  Google Scholar 

  • DC McIntyre (1981) Catecholamines involvement in amygdala kindling of the rat JA Wada (Eds) Kindling Raven Press New York 67–80

    Google Scholar 

  • DC McIntyre RJ Racine (1986) ArticleTitleKindling mechanisms: current progress on an experimental epilepsy model Prog Neurobiol 27 1–12 Occurrence Handle3526412 Occurrence Handle1:STN:280:DyaL283ovVSrtA%3D%3D

    PubMed  CAS  Google Scholar 

  • DC McIntyre RK Wong (1986) ArticleTitleCellular and synaptic properties of amygdala-kindled pyriform cortex in vitro J Neurophysiol 55 1295–1307 Occurrence Handle3016209 Occurrence Handle1:STN:280:DyaL283otVKntg%3D%3D

    PubMed  CAS  Google Scholar 

  • MI Miranda RT LaLumiere TV Buen F Bermudez-Rattoni JL McGaugh (2003) ArticleTitleBlockade of noradrenergic receptors in the basolateral amygdala impairs taste memory Eur J Neurosci 18 2605–2610 Occurrence Handle14622162 Occurrence Handle1:STN:280:DC%2BD3srmtVGmsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • P Mohapel C Dufresne ME Kelly DC McIntyre (1996) ArticleTitleDifferential sensitivity of various temporal lobe structures in the rat to kindling and status epilepticus induction Epilepsy Res 23 179–187 Occurrence Handle8739121 Occurrence Handle1:STN:280:DyaK28zitlGltg%3D%3D

    PubMed  CAS  Google Scholar 

  • K Morimoto M Fahnestock RJ Racine (2004) ArticleTitleKindling and status epilepticus models of epilepsy: rewiring the brain Prog Neurobiol 73 1–60 Occurrence Handle15193778 Occurrence Handle1:CAS:528:DC%2BD2cXkvVeitbY%3D

    PubMed  CAS  Google Scholar 

  • DJ Nutt AL Malizia (2004) ArticleTitleStructural and functional brain changes in posttraumatic stress disorder J Clin Psychiatry 65 IssueIDSuppl 1 11–17 Occurrence Handle14728092

    PubMed  Google Scholar 

  • E Palma V Esposito AM Mileo G Di Gennaro P Quarato F Giangaspero C Scoppetta P Onorati F Trettel R Miledi F Eusebi (2002) ArticleTitleExpression of human epileptic temporal lobe neurotransmitter receptors in Xenopus oocytes: An innovative approach to study epilepsy Proc Natl Acad Sci USA 99 15078–15083 Occurrence Handle12409614 Occurrence Handle1:CAS:528:DC%2BD38Xpt1yru7w%3D

    PubMed  CAS  Google Scholar 

  • A Pitkanen (2000) Connectivity of the rat amygdaloid complex JP Aggleton (Eds) The amygdala: a functional analysis OUP Oxford 33–99

    Google Scholar 

  • A Pitkanen M Pikkarainen N Nurminen A Ylinen (2000) ArticleTitleReciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review Ann NY Acad Sci 911 369–391 Occurrence Handle10911886 Occurrence Handle1:STN:280:DC%2BD3czptVCluw%3D%3D Occurrence Handle10.1111/j.1749-6632.2000.tb06738.x

    Article  PubMed  CAS  Google Scholar 

  • A Pitkanen V Savander JE LeDoux (1997) ArticleTitleOrganization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala Trends Neurosci 20 517–523 Occurrence Handle9364666 Occurrence Handle1:CAS:528:DyaK2sXnt1CrtbY%3D

    PubMed  CAS  Google Scholar 

  • A Pitkanen TP Sutula (2002) ArticleTitleIs epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy Lancet Neurol 1 173–181 Occurrence Handle12849486

    PubMed  Google Scholar 

  • A Pitkanen J Tuunanen R Kalviainen K Partanen T Salmenpera (1998) ArticleTitleAmygdala damage in experimental and human temporal lobe epilepsy Epilepsy Res 32 233–253 Occurrence Handle9761324 Occurrence Handle1:STN:280:DyaK1cvjt1Cqsw%3D%3D

    PubMed  CAS  Google Scholar 

  • RK Pitman LM Shin SL Rauch (2001) ArticleTitleInvestigating the pathogenesis of posttraumatic stress disorder with neuroimaging J Clin Psychiatry 62 IssueIDSuppl 17 47–54 Occurrence Handle11495097

    PubMed  Google Scholar 

  • A Quattrone V Crunelli R Samanin (1978) ArticleTitleSeizure susceptibility and anticonvulsant activity of carbamazepine, diphenylhydantoin and phenobarbital in rats with selective depletions of brain monoamines Neuropharmacology 17 643–647 Occurrence Handle692823 Occurrence Handle1:CAS:528:DyaE1MXhtFGjt7Y%3D

    PubMed  CAS  Google Scholar 

  • A Quattrone R Samanin (1977) ArticleTitleDecreased anticonvulsant activity of carbamazepine in 6-hydroxydopamine-treated rats Eur J Pharmacol 41 336–336 Occurrence Handle837975 Occurrence Handle1:STN:280:DyaE2s7hsF2mtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • GL Quirarte R Galvez B Roozendaal JL McGaugh (1998) ArticleTitleNorepinephrine release in the amygdala in response to footshock and opioid peptidergic drugs Brain Res 808 134–140 Occurrence Handle9767150 Occurrence Handle1:CAS:528:DyaK1cXmt1enu70%3D

    PubMed  CAS  Google Scholar 

  • RJ Racine G Paxinos JM Mosher EW Kairiss (1988) ArticleTitleThe effects of various lesions and knife-cuts on septal and amygdala kindling in the rat Brain Res 454 264–274 Occurrence Handle3409010 Occurrence Handle1:STN:280:DyaL1czhtVeisg%3D%3D

    PubMed  CAS  Google Scholar 

  • Rankin F, Aroniadou-Anderjaska V, Li H, Braga MF (2005) Overexposure to norepinephrine (NE) impairs the a1a adrenoceptor-mediated facilitation of GABA release in the basolateral amygdala (BLA). Soc Neurosci 272.4 (abstract)

  • SL Rauch PJ Whalen LM Shin SC McInerney ML Macklin NB Lasko SP Orr RK Pitman (2000) ArticleTitleExaggerated amygdala response to masked facial stimuli in posttraumatic stress disorder: a functional MRI study Biol Psychiatry 47 769–776 Occurrence Handle10812035 Occurrence Handle1:STN:280:DC%2BD3c3nslKisg%3D%3D

    PubMed  CAS  Google Scholar 

  • MA Rogawski D Gryder D Castaneda W Yonekawa MK Banks H Lia (2003) ArticleTitleGluR5 kainate receptors, seizures, and the amygdala Ann NY Acad Sci 985 150–162 Occurrence Handle12724156 Occurrence Handle1:CAS:528:DC%2BD3sXjvVegsrs%3D Occurrence Handle10.1111/j.1749-6632.2003.tb07079.x

    Article  PubMed  CAS  Google Scholar 

  • P Sah ES Faber M Lopez De Armentia J Power (2003) ArticleTitleThe amygdaloid complex: anatomy and physiology Physiol Rev 83 803–834 Occurrence Handle12843409 Occurrence Handle1:CAS:528:DC%2BD3sXmtVGmsLw%3D

    PubMed  CAS  Google Scholar 

  • SJ Sara C Dyon-Laurent A Herve (1995) ArticleTitleNovelty seeking behavior in the rat is dependent upon the integrity of the noradrenergic system Brain Res Cogn Brain Res 2 181–187 Occurrence Handle7580400 Occurrence Handle1:CAS:528:DyaK2MXnvValsr8%3D

    PubMed  CAS  Google Scholar 

  • A Saukkonen R Kalviainen K Partanen P Vainio P Riekkinen A Pitkanen (1994) ArticleTitleDo seizures cause neuronal damage? A MRI study in newly diagnosed and chronic epilepsy Neuroreport 6 219–223 Occurrence Handle7703420 Occurrence Handle1:STN:280:DyaK2M3hvVSqug%3D%3D

    PubMed  CAS  Google Scholar 

  • HH Schiffer GT Swanson SF Heinemann (1997) ArticleTitleRat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate Neuron 19 1141–1146 Occurrence Handle9390526 Occurrence Handle1:CAS:528:DyaK2sXnvFeqsrk%3D

    PubMed  CAS  Google Scholar 

  • F Schneider U Weiss C Kessler JB Salloum S Posse W Grodd HW Muller-Gartner (1998) ArticleTitleDifferential amygdala activation in schizophrenia during sadness Schizophr Res 34 133–142 Occurrence Handle9850979 Occurrence Handle1:STN:280:DyaK1M%2Fmsl2ltw%3D%3D

    PubMed  CAS  Google Scholar 

  • B Schulz M Fendt HU Schnitzler (2002) ArticleTitleClonidine injections into the lateral nucleus of the amygdala block acquisition and expression of fear-potentiated startle Eur J Neurosci 15 151–157 Occurrence Handle11860515

    PubMed  Google Scholar 

  • NR Selden TW Robbins BJ Everitt (1990) ArticleTitleEnhanced behavioral conditioning to context and impaired behavioral and neuroendocrine responses to conditioned stimuli following ceruleocortical noradrenergic lesions: support for an attentional hypothesis of central noradrenergic function J Neurosci 10 531–539 Occurrence Handle2303858 Occurrence Handle1:CAS:528:DyaK3cXhtFaksL0%3D

    PubMed  CAS  Google Scholar 

  • RJ Servatius JE Ottenweller BH Natelson (1995) ArticleTitleDelayed startle sensitization distinguishes rats exposed to one or three stress sessions: further evidence toward an animal model of PTSD Biol Psychiatry 38 539–546 Occurrence Handle8562666 Occurrence Handle1:STN:280:DyaK287itVeqtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • YI Sheline DM Barch JM Donnelly JM Ollinger AZ Snyder MA Mintun (2001) ArticleTitleIncreased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study Biol Psychiatry 50 651–658 Occurrence Handle11704071 Occurrence Handle1:CAS:528:DC%2BD3MXotFSmu7c%3D

    PubMed  CAS  Google Scholar 

  • I Smolders ZA Bortolotto VR Clarke R Warre GM Khan MJ O’Neill PL Ornstein D Bleakman A Ogden B Weiss JP Stables KH Ho G Ebinger GL Collingridge D Lodge Y Michotte (2002) ArticleTitleAntagonists of GLU(K5)-containing kainate receptors prevent pilocarpine-induced limbic seizures Nat Neurosci 5 796–804 Occurrence Handle12080343 Occurrence Handle1:CAS:528:DC%2BD38XlsFaqu7w%3D

    PubMed  CAS  Google Scholar 

  • B Sommer N Burnashev TA Verdoorn K Keinanen B Sakmann PH Seeburg (1992) ArticleTitleA glutamate receptor channel with high affinity for domoate and kainate Embo J 11 1651–1656 Occurrence Handle1373382 Occurrence Handle1:CAS:528:DyaK38Xit1yku7g%3D

    PubMed  CAS  Google Scholar 

  • B Sommer M Kohler R Sprengel PH Seeburg (1991) ArticleTitleRNA editing in brain controls a determinant of ion flow in glutamate-gated channels Cell 67 11–19 Occurrence Handle1717158 Occurrence Handle1:CAS:528:DyaK38Xhs1Kh

    PubMed  CAS  Google Scholar 

  • SC Stanford (1995) ArticleTitleCentral noradrenergic neurones and stress Pharmacol Ther 68 297–242 Occurrence Handle8719972 Occurrence Handle1:CAS:528:DyaK28XhtFOmsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • L Stefanacci CR Farb A Pitkanen G Go JE LeDoux DG Amaral (1992) ArticleTitleProjections from the lateral nucleus to the basal nucleus of the amygdala: a light and electron microscopic PHA-L study in the rat J Comp Neurol 323 586–601 Occurrence Handle1430325 Occurrence Handle1:STN:280:DyaK3s%2FlsFGqsg%3D%3D

    PubMed  CAS  Google Scholar 

  • MB Stein PR Goldin J Sareen LT Zorrilla GG Brown (2002) ArticleTitleIncreased amygdala activation to angry and contemptuous faces in generalized social phobia Arch Gen Psychiatry 59 1027–1034 Occurrence Handle12418936

    PubMed  Google Scholar 

  • EA Stone BS McEwen AS Herrera KD Carr (1987) ArticleTitleRegulation of alpha and beta components of noradrenergic cyclic AMP response in cortical slices Eur J Pharmacol 141 347–356 Occurrence Handle2822449 Occurrence Handle1:CAS:528:DyaL2sXmtFahtbw%3D

    PubMed  CAS  Google Scholar 

  • EA Stone JE Platt AS Herrera KL Kirk (1986) ArticleTitleEffect of repeated restraint stress, desmethylimipramine or adrenocorticotropin on the alpha and beta adrenergic components of the cyclic AMP response to norepinephrine in rat brain slices J Pharmacol Exp Ther 237 702–707 Occurrence Handle3012065 Occurrence Handle1:CAS:528:DyaL28XktlKhsLg%3D

    PubMed  CAS  Google Scholar 

  • BA Strange RJ Dolan (2004) ArticleTitleBeta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses Proc Natl Acad Sci USA 101 11454–11458 Occurrence Handle15269349 Occurrence Handle1:CAS:528:DC%2BD2cXmvVKgurg%3D

    PubMed  CAS  Google Scholar 

  • T Straube HJ Mentzel WH Miltner (2005) ArticleTitleCommon and distinct brain activation to threat and safety signals in social phobia Neuropsychobiology 52 163–168 Occurrence Handle16137995

    PubMed  Google Scholar 

  • P Szot D Weinshenker JM Rho TW Storey PA Schwartzkroin (2001) ArticleTitleNorepinephrine is required for the anticonvulsant effect of the ketogenic diet Brain Res Dev Brain Res 129 211–214 Occurrence Handle11506865 Occurrence Handle1:CAS:528:DC%2BD3MXlvFWlur4%3D

    PubMed  CAS  Google Scholar 

  • M Tanaka M Yoshida H Emoto H Ishii (2000) ArticleTitleNoradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies Eur J Pharmacol 405 397–406 Occurrence Handle11033344 Occurrence Handle1:CAS:528:DC%2BD3cXnt1Siur4%3D

    PubMed  CAS  Google Scholar 

  • NR Temkin GR Davis (1984) ArticleTitleStress as a risk factor for seizures among adults with epilepsy Epilepsia 25 450–456 Occurrence Handle6745217 Occurrence Handle1:STN:280:DyaL2c3mtFelsw%3D%3D

    PubMed  CAS  Google Scholar 

  • G Ullal M Fahnestock R Racine (2005) ArticleTitleTime-dependent effect of kainate-induced seizures on glutamate receptor GluR5, GluR6, and GluR7 mRNA and protein expression in rat hippocampus Epilepsia 46 616–623 Occurrence Handle15857425 Occurrence Handle1:CAS:528:DC%2BD2MXkslymsr0%3D

    PubMed  CAS  Google Scholar 

  • M Usher JD Cohen D Servan-Schreiber J Rajkowski G Aston-Jones (1999) ArticleTitleThe role of locus coeruleus in the regulation of cognitive performance Science 283 549–554 Occurrence Handle9915705 Occurrence Handle1:CAS:528:DyaK1MXoslCksA%3D%3D

    PubMed  CAS  Google Scholar 

  • M Vignes GL Collingridge (1997) ArticleTitleThe synaptic activation of kainate receptors Nature 388 179–182 Occurrence Handle9217158 Occurrence Handle1:CAS:528:DyaK2sXksFWls7o%3D

    PubMed  CAS  Google Scholar 

  • G Villarreal CY King (2001) ArticleTitleBrain imaging in posttraumatic stress disorder Semin Clin Neuropsychiatry 6 131–145 Occurrence Handle11296313 Occurrence Handle1:STN:280:DC%2BD3MzmvFyisw%3D%3D

    PubMed  CAS  Google Scholar 

  • SB Waller GG Buterbaugh (1985) ArticleTitleConvulsive thresholds and severity and the anticonvulsant effect of phenobarbital and phenytoin in adult rats administered 6-hydroxydopamine or 5,7-dihydroxytryptamine during postnatal development Pharmacol Biochem Behav 23 473–478 Occurrence Handle3931103 Occurrence Handle1:CAS:528:DyaL2MXlslWqsL0%3D

    PubMed  CAS  Google Scholar 

  • D Weinshenker P Szot (2002) ArticleTitleThe role of catecholamines in seizure susceptibility: new results using genetically engineered mice Pharmacol Ther 94 213–233 Occurrence Handle12113799 Occurrence Handle1:CAS:528:DC%2BD38XltV2qtrw%3D

    PubMed  CAS  Google Scholar 

  • D Weinshenker SS White MA Javors RD Palmiter P Szot (2002) ArticleTitleRegulation of norepinephrine transporter abundance by catecholamines and desipramine in vivo Brain Res 946 239–246 Occurrence Handle12137927 Occurrence Handle1:CAS:528:DC%2BD38Xls1ans7Y%3D

    PubMed  CAS  Google Scholar 

  • LE White JL Price (1993a) ArticleTitleThe functional anatomy of limbic status epilepticus in the rat. I. Patterns of 14C-2-deoxyglucose uptake and Fos immunocytochemistry J Neurosci 13 4787–4809 Occurrence Handle1:CAS:528:DyaK2cXnsVKqsA%3D%3D

    CAS  Google Scholar 

  • LE White JL Price (1993b) ArticleTitleThe functional anatomy of limbic status epilepticus in the rat. II. The effects of focal deactivation J Neurosci 13 4810–4830 Occurrence Handle1:STN:280:DyaK2c%2FksF2isw%3D%3D

    CAS  Google Scholar 

  • AM Williams ML Nguyen DA Morilak (1997) ArticleTitleCo-localization of alpha1D adrenergic receptor mRNA with mineralocorticoid and glucocorticoid receptor mRNA in rat hippocampus J Neuroendocrinol 9 113–119 Occurrence Handle9041364 Occurrence Handle1:CAS:528:DyaK2sXht1Ggs7Y%3D

    PubMed  CAS  Google Scholar 

  • CL Williams D Men EC Clayton (2000) ArticleTitleThe effects of noradrenergic activation of the nucleus tractus solitarius on memory and in potentiating norepinephrine release in the amygdala Behav Neurosci 114 1131–1144 Occurrence Handle11142645 Occurrence Handle1:CAS:528:DC%2BD3MXitFWitQ%3D%3D

    PubMed  CAS  Google Scholar 

  • M Yang J Ruan M Voller J Schalken MC Michel (1999) ArticleTitleDifferential regulation of human alpha1-adrenoceptor subtypes Naunyn Schmiedebergs Arch Pharmacol 359 439–446 Occurrence Handle10431753 Occurrence Handle1:CAS:528:DyaK1MXjs1Gmsbc%3D

    PubMed  CAS  Google Scholar 

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Aroniadou-Anderjaska, V., Qashu, F. & Braga, M. Mechanisms regulating GABAergic inhibitory transmission in the basolateral amygdala: implications for epilepsy and anxiety disorders. Amino Acids 32, 305–315 (2007). https://doi.org/10.1007/s00726-006-0415-x

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