Amygdala-Specific Reduction of α1-GABA A Receptors Disrupts the Anticonvulsant, Locomotor, and Sedative, But Not Anxiolytic, Effects of Benzodiazepines in Mice
Open accessAbstract
The heterogeneity and distribution of GABA(A) receptor subunits mediates differential roles in behavior. It is thought that particular behavioral responses to benzodiazepine (BZ) ligands might be associated with an action at a regionally defined receptor subtype. However, the role of specific GABA(A) receptor subtypes in particular brain regions is less clear. Such detailed knowledge of regional alpha1-GABA(A) receptor function will advance our understanding of the neural circuitry underlying the role of GABA(A) receptors and the effects of GABA(A)-modulating drugs on behavior. By combining inducible, site-specific alpha1 subunit deletion, using a lentivirus expressing Cre-recombinase in mice with the alpha1 subunit gene flanked by loxP sites, we examine baseline and pharmacological effects of deletion of amygdala alpha1-GABA(A) receptors. We find that amygdala-specific reduction of alpha1 receptor subunits does not affect mRNA or protein levels of amygdala alpha2 or alpha3 subunit receptors. Nor does this inducible reduction affect baseline locomotion or measures of anxiety. However, we also find that this inducible, site-specific deletion does disrupt the normal sedative-locomotor inhibition as well as the anticonvulsive effects, of two distinct BZ-site ligands, diazepam and zolpidem, which is relatively alpha1-subunit selective. These data, using inducible, region and subunit-specific deletion, combined with pharmacogenetic approaches, demonstrate that amygdala expression of the alpha1-GABA(A) receptor subunit is required for normal BZ effects on sedation, locomotion, and seizure inhibition, but not for anxiolysis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
α1GABAARs of the BLA do not seem important for anxiety-related behaviors in the elevated plus maze.
“While playing such a substantial role in the acquisition and expression of conditioned fear, α1GABAARs of the BLA do not seem to be important for anxiety-related behaviors in the elevated plus maze (see Box 5) [25]”
From An emerging circuit pharmacology of GABAA receptors (2018) · cites this paper as [25]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review.
Prut, L., & Belzung, C. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01272-x · Cited by 3,190 · see citing works
Pellow, S., & File, S. E. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90552-6 · Cited by 1,534 · see citing works
Drug Discovery and Evaluation: Pharmacological Assays
(2014) · Springer eBooks · doi:10.1007/978-3-642-27728-3 · Cited by 1,408 · see citing works
GABAA receptors: immunocytochemical distribution of 13 subunits in the adult rat brain
Pirker, S., Schwarzer, C., Wieselthaler, A., Sieghart, W., & Sperk, G. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00442-5 · Cited by 1,344 · see citing works
Fritschy, J., & Mohler, H. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590111 · Cited by 1,244 · see citing works
Which GABAA-receptor subtypes really occur in the brain?
McKernan, R. M., & Whiting, P. J. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)80023-3 · Cited by 1,222 · see citing works
Barnard, E. A., Skolnick, P., Olsen, R. W., Möhler, H., Sieghart, W., Biggio, G., Bræstrup, C., Bateson, A. N., & Langer, S. Z. (1998) · PubMed · Cited by 1,204 · see citing works
Benzodiazepine actions mediated by specific γ-aminobutyric acidA receptor subtypes
Rudolph, U., Crestani, F., Benke, D., Brünig, I., Benson, J. A., Fritschy, J.-M., Martin, J. R., Bluethmann, H., & Möhler, H. (1999) · Nature · doi:10.1038/44579 · Cited by 1,172 · see citing works
A review of the validity and variability of the Elevated Plus-Maze as an animal model of anxiety
Hogg, S. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02126-4 · Cited by 1,169 · see citing works
Anxiety, defence and the elevated plus-maze.
Rodgers, R., & Dalvi, A. (1997) · Neuroscience and Biobehavioral Reviews · doi:10.1016/s0149-7634(96)00058-9 · Cited by 1,028 · see citing works
Production and purification of lentiviral vectors
Tiscórnia, G., Singer, O., & Verma, I. M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.37 · Cited by 974 · see citing works
Molecular and neuronal substrate for the selective attenuation of anxiety
Löw, K., Crestani, F., Keist, R., Benke, D., Brünig, I., Benson, J. A., Fritschy, J.-M., Rülicke, T., Bluethmann, H., Möhler, H., et al. (2000) · Science · doi:10.1126/science.290.5489.131 · Cited by 946 · see citing works
McKernan, R. M., Rosahl, T. W., Reynolds, D. S., Sur, C., Wafford, K. A., Atack, J. R., Farrar, S., Myers, J., Cook, G., Ferris, P., et al. (2000) · Nature Neuroscience · doi:10.1038/75761 · Cited by 944 · see citing works
Subunit Composition, Distribution and Function of GABA-A Receptor Subtypes
Sieghart, W., & Sperk, G. (2002) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026023393507 · Cited by 914 · see citing works
A new benzodiazepine pharmacology
Möhler, H., Fritschy, J. M., & Rudolph, U. (2002) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.300.1.2 · Cited by 716 · see citing works
Barnard, E. A., Skolnick, P., Olsen, R. W., Möhler, H., Sieghart, W., Biggio, G., Bræstrup, C., Bateson, A. N., & Langer, S. Z. (1998) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01363-2 · Cited by 711 · see citing works
Heldt, S. A., Stanek, L., Chhatwal, J. P., & Ressler, K. J. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001957 · Cited by 684 · see citing works
Self-citationMehta, A. K., & Ticku, M. K. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00052-6 · Cited by 611 · see citing works
Tiscórnia, G., Singer, O., Ikawa, M., & Verma, I. M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437912100 · Cited by 540 · see citing works
Rudolph, U., & Möhler, H. (2004) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.44.101802.121429 · Cited by 518 · see citing works
Löscher, W. (2002) · Epilepsy Research · doi:10.1016/s0920-1211(02)00073-6 · Cited by 510 · see citing works
γ‐Aminobutyric AcidA Receptor α5‐Subunit Creates Novel Type II Benzodiazepine Receptor Pharmacology
Pritchett, D. B., & Seeburg, P. H. (1990) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1990.tb01237.x · Cited by 503 · see citing works
The diversity of GABAA receptors
Hevers, W., & Lüddens, H. (1998) · Molecular Neurobiology · doi:10.1007/bf02741459 · Cited by 482 · see citing works
Isolation and culture of adult rat hippocampal neurons
Brewer, G. J. (1997) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(96)00136-7 · Cited by 438 · see citing works
GABA A receptor subtypes: from pharmacology to molecular biology
Burt, D. R., & Kamatchi, G. L. (1991) · The FASEB Journal · doi:10.1096/fasebj.5.14.1661244 · Cited by 425 · see citing works
Vagaries of conditional gene targeting
Schmidt‐Supprian, M., & Rajewsky, K. (2007) · Nature Immunology · doi:10.1038/ni0707-665 · Cited by 417 · see citing works
GABAA receptor diversity and pharmacology
Möhler, H. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0284-3 · Cited by 359 · see citing works
Structure, Pharmacology, and Function of GABAA Receptor Subtypes
Sieghart, W. (2006) · Advances in pharmacology · doi:10.1016/s1054-3589(06)54010-4 · Cited by 321 · see citing works
Vicini, S., Ferguson, C., Prybylowski, K., Kralic, J. E., Morrow, A. L., & Homanics, G. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03009.2001 · Cited by 309 · see citing works
Mechanism of action of the hypnotic zolpidem in vivo
Crestani, F., Martin, J. R., Möhler, H., & Rudolph, U. (2000) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703717 · Cited by 307 · see citing works
Structure and subunit composition of GABAA receptors
Sieghart, W., Fuchs, K., Tretter, V, Ebert, V, Jechlinger, M., Höger, H., & Adamiker, D. (1999) · Neurochemistry International · doi:10.1016/s0197-0186(99)00045-5 · Cited by 306 · see citing works
Zolpidem, a novel nonbenzodiazepine hypnotic. I. Neuropharmacological and behavioral effects.
Depoortere, H., Živković, B., Lloyd, K. G., Sanger, D. J., Perrault, G., Langer, S. Z., & Bartholini, G. (1986) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24899-6 · Cited by 282 · see citing works
Effects of centrally administered anxiolytic compounds in animal models of anxiety
Menard, J. L., & Treit, D. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(98)00056-6 · Cited by 280 · see citing works
Wafford, K. A., Thompson, S. A., Thomas, D., Sikela, J. M., Wilcox, A. S., & Whiting, P. J. (1996) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09339-3 · Cited by 268 · see citing works
Cloning, pharmacological characteristics and expression pattern of the rat GABAA receptor α4 subunit
Wisden, W., Herb, A., Wieland, H., KEINÄNEN, K. P., Lüddens, H., & Seeburg, P. H. (1991) · FEBS Letters · doi:10.1016/0014-5793(91)81076-k · Cited by 260 · see citing works
Macdonald, R. L., & Barker, J. L. (1977) · Nature · doi:10.1038/267720a0 · Cited by 259 · see citing works
Comparative Pharmacokinetics and Pharmacodynamics of Short-Acting Hypnosedatives
Drover, D. R. (2004) · Clinical Pharmacokinetics · doi:10.2165/00003088-200443040-00002 · Cited by 248 · see citing works
Hodges, H., Green, S., & Glenn, B. (1987) · Psychopharmacology · doi:10.1007/bf00176484 · Cited by 242 · see citing works
Loss of the Major GABA A Receptor Subtype in the Brain Is Not Lethal in Mice
Sur, C., Wafford, K. A., Reynolds, D. S., Hadingham, K. L., Bromidge, F. A., Macaulay, A. J., Collinson, N., O’Meara, G. F., Howell, O. W., Newman, R. J., et al. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-10-03409.2001 · Cited by 229 · see citing works
Löscher, W., & Schmidt, D. (1994) · Epilepsy Research · doi:10.1016/0920-1211(94)90012-4 · Cited by 221 · see citing works
Regulation of Synaptic Plasticity Genes during Consolidation of Fear Conditioning
Ressler, K. J., Paschall, G. Y., Zhou, X., & Davis, M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-18-07892.2002 · Cited by 217 · see citing works
Self-citationPesold, C., & Treit, D. (1995) · Brain Research · doi:10.1016/0006-8993(94)01318-c · Cited by 208 · see citing works
Molecular and Pharmacological Characterization of GABAA Receptor α1 Subunit Knockout Mice
Kralic, J. E., Korpi, E. R., O’Buckley, T. K., Homanics, G. E., & Morrow, A. L. (2002) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.036665 · Cited by 201 · see citing works
Benson, J. A., Löw, K., Keist, R., Möhler, H., & Rudolph, U. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00803-5 · Cited by 184 · see citing works
Raol, Y. H., Lund, I. V., Bandyopadhyay, S., Zhang, G., Roberts, D. S., Wolfe, J. H. N., Russek, S. J., & Brooks‐Kayal, A. R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3329-06.2006 · Cited by 176 · see citing works
The Pharmacology and Mechanisms of Action of New Generation, Non-Benzodiazepine Hypnotic Agents
Sanger, D. J. (2004) · CNS Drugs · doi:10.2165/00023210-200418001-00004 · Cited by 169 · see citing works
Stoichiometry of a recombinant GABAA receptor deduced from mutation-induced rectification
Backus, K. H., Arigoni, M., Drescher, U., Scheurer, L., Malherbe, P., Möhler, H., & Benson, J. A. (1993) · Neuroreport · doi:10.1097/00001756-199312000-00026 · Cited by 168 · see citing works
Kralic, J. E., O’Buckley, T. K., Khisti, R. T., Hodge, C. W., Homanics, G. E., & Morrow, A. L. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00174-0 · Cited by 166 · see citing works
RO4938581, a novel cognitive enhancer acting at GABAA α5 subunit-containing receptors
Ballard, T. M., Knoflach, F., Prinssen, E. P. M., Borroni, E., Vivian, J. A., Basile, J., Gasser, R., Moreau, J., Wettstein, J. G., Buettelmann, B., et al. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1357-7 · Cited by 156 · see citing works
GABAA Receptors: Subtypes, Regional Distribution, and Function
Nutt, D. (2006) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.26525 · Cited by 141 · see citing works
Kralic, J. E., Sidler, C., Parpan, F., Homanics, G. E., Morrow, A. L., & Fritschy, J. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20866 · Cited by 135 · see citing works
Modulation of rhythmic brain activity by diazepam: GABA A receptor subtype and state specificity
Kopp, C., Rudolph, U., Löw, K., & Tobler, I. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306975101 · Cited by 132 · see citing works
Anxioselective Compounds Acting at the GABAA Receptor Benzodiazepine Binding Site
Atack, J. R. (2003) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1568007033482841 · Cited by 130 · see citing works
Heldt, S. A., & Ressler, K. J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05970.x · Cited by 125 · see citing works
Self-citationComparison of the pharmacological profiles of the hypnotic drugs, zaleplon and zolpidem
Sanger, D. J., Morel, E., & Perrault, G. (1996) · European Journal of Pharmacology · doi:10.1016/0014-2999(96)00510-9 · Cited by 108 · see citing works
Functional mapping of GABAA receptor subtypes in the amygdala
Marowsky, A., Fritschy, J., & Vogt, K. E. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03574.x · Cited by 107 · see citing works
Hadingham, K. L., Garrett, E. M., Wafford, K. A., Bain, C., HEAVENS, R. P., SIRINATHSINGHJI, D. J. S., & Whiting, P. J. (1996) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)08706-1 · Cited by 99 · see citing works
Nunes‐de‐Souza, R. L., Canto‐de‐Souza, A., da-Costa, M., Fornari, R. V., Graeff, F. G., & Pelá, I. R. (2000) · Psychopharmacology · doi:10.1007/s002130000428 · Cited by 96 · see citing works
Engin, E., & Treit, D. (2008) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2008.03.020 · Cited by 90 · see citing works
Sanders, S., & Shekhar, A. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00183-4 · Cited by 88 · see citing works
Griebel, G., Sanger, D. J., & Perrault, G. (1996) · Psychopharmacology · doi:10.1007/bf02246664 · Cited by 85 · see citing works
l-NAME inhibits pentylenetetrazole and strychnine-induced seizures in mice
Kaputlu, I., & Uzbay, T. I. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01496-5 · Cited by 82 · see citing works
Griebel, G., Perrault, G., Simiand, J., Cohen, C., Granger, P., Depoortere, H., Françon, D., Avenet, P., Schoemaker, H., Evanno, Y., et al. (2003) · CNS Drug Reviews · doi:10.1111/j.1527-3458.2003.tb00241.x · Cited by 76 · see citing works
Smith, T. (2001) · PubMed · Cited by 75 · see citing works
Bosman, L. W. J., Heinen, K., Spijker, S., & Brussaard, A. B. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00084.2005 · Cited by 72 · see citing works
Petersen, E. N., Bræstrup, C., & Scheel‐Krüger, J. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90552-x · Cited by 71 · see citing works
Memory Effects of Benzodiazepines: Memory Stages and Types Versus Binding‐Site Subtypes
Savić, M. M., Obradovic, D. I., Ugrešić, N. D., & Bokonjić, D. (2005) · Neural Plasticity · doi:10.1155/np.2005.289 · Cited by 64 · see citing works
Do preclinical seizure models preselect certain adverse effects of antiepileptic drugs
Meldrum, B. S. (2002) · Epilepsy Research · doi:10.1016/s0920-1211(02)00066-9 · Cited by 63 · see citing works
Kaufmann, W. A., Humpel, C., Alheid, G. F., & Marksteiner, J. (2003) · Brain Research · doi:10.1016/s0006-8993(02)04082-9 · Cited by 62 · see citing works
Crestani, F., Assandri, R., Täuber, M., Martin, J. R., & Rudolph, U. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00159-4 · Cited by 62 · see citing works
Resolving differences in GABAA receptor mutant mouse studies
Crestani, F., Martin, J. R., Möhler, H., & Rudolph, U. (2000) · Nature Neuroscience · doi:10.1038/80553 · Cited by 59 · see citing works
Griebel, G., Perrault, G., Simiand, J., Cohen, C., Granger, P., Decobert, M., Françon, D., Avenet, P., Depoortere, H., Tan, S., et al. (2001) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29437-4 · Cited by 59 · see citing works
Ligands for the Benzodiazepine Binding Site - a Survey
Teuber, L., Wätjen, F., & Jensen, L. H. (1999) · Current Pharmaceutical Design · doi:10.2174/138161280505230110100242 · Cited by 57 · see citing works
Role of amygdaloid nuclei in the anxiolytic effects of benzodiazepines in rats
Green, S., & Vale, A. L. (1992) · Behavioural Pharmacology · doi:10.1097/00008877-199206000-00010 · Cited by 54 · see citing works
Nevins, M. E., & Arnolde, S. M. (1989) · Brain Research · doi:10.1016/0006-8993(89)91695-8 · Cited by 53 · see citing works
Tietz, E. I., Huang, X., Chen, S., & Ferencak, W. F. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00516-8 · Cited by 51 · see citing works
Gasser, E. M. S., Duveau, V., Prenosil, G., & Fritschy, J. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05558.x · Cited by 44 · see citing works
Ogris, W., Lehner, R., Fuchs, K., Furtmüller, B., Höger, H., Homanics, G. E., & Sieghart, W. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03509.x · Cited by 43 · see citing works
Cortical Glutamatergic Neurons Mediate the Motor Sedative Action of Diazepam
Zeller, A., Crestani, F., Camenisch, I., Iwasato, T., Itohara, S., Fritschy, J., & Rudolph, U. (2007) · Molecular Pharmacology · doi:10.1124/mol.107.038828 · Cited by 36 · see citing works
Regional and age specific effects of zolpidem microinfusions in the substantia nigra on seizures
Velı́šková, J., Löscher, W., & Moshé, S. L. (1998) · Epilepsy Research · doi:10.1016/s0920-1211(97)00096-x · Cited by 32 · see citing works
Amygdaloid kindling with bicuculline methiodide in rats
Uemura, S., & Kimura, H. (1988) · Experimental Neurology · doi:10.1016/0014-4886(88)90230-0 · Cited by 28 · see citing works
Cunha, C. D., Wolfman, C., de Stein, M. L., Ruschel, A. C., Izquierdo, I., & Medina, J. H. (1992) · PubMed · Cited by 24 · see citing works
Heldt, S. A., & Ressler, K. J. (2006) · Behavioural Pharmacology · doi:10.1097/01.fbp.0000224386.86615.e0 · Cited by 17 · see citing works
Self-citationJasnow, A. M., Rainnie, D. G., Maguschak, K. A., Chhatwal, J. P., & Ressler, K. J. (2009) · Methods in molecular biology · doi:10.1007/978-1-59745-559-6_13 · Cited by 15 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 2
- Rudolph U Crestani F Benke D Brunig I Benson JA Fritschy J-M Martin JR Bluethmann H Mohler H 1999b Benzodiazepine actions mediated by specific [gamma]-aminobutyric acidA receptor subtypes Nature 401 796 800 10548105
- Sanger DJ Morel E Perrault G 1996b Comparison of the pharmacological profiles of the hypnotic drugs, zaleplon and zolpidem European Journal of Pharmacology 313 35 42 8905326
Cited by
Sorted by citations
Inhibition in the amygdala anxiety circuitry
Babaev, O., Chatain, C. P., & Krueger‐Burg, D. (2018) · Experimental & Molecular Medicine · doi:10.1038/s12276-018-0063-8 · Cited by 311 · see citing works
An emerging circuit pharmacology of GABAA receptors
Engin, E., Benham, R. S., & Rudolph, U. (2018) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.04.003 · Cited by 225 · see citing works
Saari, T. I., Uusi‐Oukari, M., Ahonen, J., & Olkkola, K. T. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.002717 · Cited by 154 · see citing works
The neurobiology of alcohol consumption and alcoholism: An integrative history
Tabakoff, B., & Hoffman, P. L. (2013) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.10.009 · Cited by 135 · see citing works
Gafford, G. M., Guo, J., Flandreau, E. I., Hazra, R., Rainnie, D. G., & Ressler, K. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119261109 · Cited by 96 · see citing works
Self-citationHeldt, S. A., Mou, L., & Ressler, K. J. (2012) · Translational Psychiatry · doi:10.1038/tp.2012.101 · Cited by 76 · see citing works
Self-citationGABAergic implications in anxiety and related disorders
Arora, I., Mal, P., Arora, P., Paul, A., & Kumar, M. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.150218 · Cited by 68 · see citing works
Bryson, A., Reid, C. A., & Petrou, S. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15769 · Cited by 63 · see citing works
Yang, L.-P., Jiang, F.-J., Wu, G.-S., Deng, K., Wen, M., Zhou, X., Hong, X., Zhu, M. X., & Luo, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136255 · Cited by 63 · see citing works
Sites of action of sleep and wake drugs: insights from model organisms
Rihel, J., & Schier, A. F. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.04.010 · Cited by 47 · see citing works
Bdnf Deletion or TrkB Impairment in Amygdala Inhibits Both Appetitive and Aversive Learning
Heldt, S. A., Zimmermann, K. S., Parker, K., Gaval‐Cruz, M., & Ressler, K. J. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4085-12.2014 · Cited by 48 · see citing works
Self-citationStefanits, H., Milenković, I., Mahr, N., Pataraia, E., Hainfellner, J. A., Kovács, G. G., Sieghart, W., Yilmazer‐Hanke, D., & Czech, T. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24337 · Cited by 48 · see citing works
The anxiolytic-like effect of rutin in rats involves GABAA receptors in the basolateral amygdala
Hernández-León, A., González-Trujano, M. E., & Fernández‐Guasti, A. (2017) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000290 · Cited by 46 · see citing works
Ethanol-Induced Plasticity of GABAA Receptors in the Basolateral Amygdala
Lindemeyer, A. K., Liang, J., Marty, V. N., Meyer, E. M., Suryanarayanan, A., Olsen, R. W., & Spigelman, I. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1297-z · Cited by 38 · see citing works
Ulk4 regulates GABAergic signaling and anxiety-related behavior
Liu, M., Fitzgibbon, M., Wang, Y., Reilly, J., Qian, X., O’Brien, T., Clapcote, S. J., Shen, S., & Roche, M. (2018) · Translational Psychiatry · doi:10.1038/s41398-017-0091-5 · Cited by 29 · see citing works
Chang, Y., Xie, X., Liu, Y., Liu, M., & Zhang, H. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116329 · Cited by 37 · see citing works
Should Benzodiazepines and Anticonvulsants Be Used During Electroconvulsive Therapy?
Tang, V. M., Pasricha, A. N., Blumberger, D. M., Voineskos, D., Pasricha, S., Mulsant, B. H., & Daskalakis, Z. J. (2017) · Journal of Ect · doi:10.1097/yct.0000000000000441 · Cited by 28 · see citing works
Cell injury and receptor expression in the epileptic human amygdala
Jafarian, M., Mousavi, S. M. M., Alipour, F., Aligholi, H., Noorbakhsh, F., Ghadipasha, M., Gharehdaghi, J., Kellinghaus, C., Kovac, S., Ghadiri, M. K., et al. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.12.017 · Cited by 26 · see citing works
Goddard, A. W. (2016) · World Journal of Psychiatry · doi:10.5498/wjp.v6.i1.43 · Cited by 24 · see citing works
GABAAα1-Mediated Plasticity in the Orbitofrontal Cortex Regulates Context-Dependent Action Selection
Swanson, A. M., Allen, A. G., Shapiro, L. P., & Gourley, S. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.292 · Cited by 21 · see citing works
Adolescent‐onset GABA Aα1 silencing regulates reward‐related decision making
Butkovich, L. M., DePoy, L. M., Allen, A. G., Shapiro, L. P., Swanson, A. M., & Gourley, S. L. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12995 · Cited by 19 · see citing works
Zhong, M., Shoemake, C. R., Fuller, A., White, D., Hanks, C., Brocksmith, D., Liu, J., Gad, S. C., Bouchard, G. F., & Stricker‐Krongrad, A. (2017) · International Journal of Toxicology · doi:10.1177/1091581816686049 · Cited by 19 · see citing works
Acetazolamide attenuates chemical-stimulated but not thermal-stimulated acute pain in mice
Sun, Y., Chen, Y., Pang, C., Wu, N., & Li, J. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2013.149 · Cited by 19 · see citing works
Sheikhi, M., Shirzadian, A., Dehdashtian, A., Amiri, S., Ostadhadi, S., Ghasemi, M., & Dehpour, A. R. (2016) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2016.07.014 · Cited by 14 · see citing works
Song, C., Xu, X.-B., He, Y., Liu, Z.-P., Wang, M., Zhang, X., Li, B., & Pan, B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060154 · Cited by 10 · see citing works
The regional and cellular distribution of GABAA receptor subunits in the human amygdala
Song, J. J., Curtis, M. A., Faull, R. L. M., & Waldvogel, H. J. (2022) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2022.102185 · Cited by 8 · see citing works
Braga, M. F. M., Juranek, J. J., Eiden, L. E., Li, Z., Figueiredo, T. H., Furtado, M. D. A., & Marini, A. M. (2022) · Amino Acids · doi:10.1007/s00726-022-03184-y · Cited by 8 · see citing works
Avolio, E., Facciolo, R. M., Alò, R., Mele, M., Carelli, A., Canonaco, A., Mosciaro, L., Talani, G., Biggio, G., Sanna, E., et al. (2013) · Neuroscience Research · doi:10.1016/j.neures.2013.07.006 · Cited by 6 · see citing works
Jia, C., Gill, W. D., Lovins, C., Brown, R. W., & Hagg, T. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100435 · Cited by 6 · see citing works
Shibasaki, M., Ishii, K., Masukawa, D., Ando, K., Ikekubo, Y., Ishikawa, Y., Shibasaki, Y., Mori, T., & Suzuki, T. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.06.001 · Cited by 4 · see citing works
Troppoli, T. A., & Thompson, S. M. (2025) · Biological Psychiatry · doi:10.1016/j.biopsych.2025.10.036 · Cited by 3 · see citing works
GABA A receptors and inhibitory neurotransmission in the amygdalar complex
Perumal, M. B., Lynch, J. W., & Sah, P. (2018) · Current Opinion in Physiology · doi:10.1016/j.cophys.2018.01.003 · Cited by 3 · see citing works
Farmacodinamia general e interacciones medicamentosas
Consolini, A. E., & Ragone, M. (2017) · doi:10.35537/10915/67056 · Cited by 2 · see citing works
Pakkhesal, S., Shakouri, M., Mosaddeghi-Heris, R., Nasab, S. K., Salehi, N., Sharafi, A. M., & Ahmadalipour, A. (2025) · Pharmacology and Therapeutics · doi:10.1016/j.pharmthera.2025.108799 · Cited by 4 · see citing works
Roeder, N. M., Powell, A., Hamilton, J. A., Richardson, B., Sharma, A., Sharafshah, A., Blum, K., Pinhasov, A., & Thanos, P. K. (2026) · Neuroscience Letters · doi:10.1016/j.neulet.2026.138558 · Cited by 1 · see citing works
Benzodiazepines for anxiety and depression: an updated overview of current use and major outcomes
Fatimi, H. E., Khalki, H., El‐Mansoury, B., Zaid, Y., & Khalki, L. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-11939-z · Cited by 1 · see citing works
Reduction of Pain Behavior by Stimulation of the Basolateral Amygdalar Nuclei in Freely Moving Rats
Onozawa, K., Izawa, Y., Abe, H., & Kawakami, Y. (2012) · Neurophysiology · doi:10.1007/s11062-012-9310-0
GABA A alpha-5 subunit manipulation of maternal separation-induced anxiety in mice
Sloley, S. S., Hwa, L. S., DeBold, J. F., Miczek, K. A., & Thesis, H. (2011)
The K + -Cl − Cotransporter KCC2 and Zolpidem
Shibasaki, M., Mori, T., & Suzuki, T. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800634-4.00031-7
Jia, C., Gill, W. D., Lovins, C., Hagg, T., & Brown, R. W. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3991834
Li, J.-K., Wang, R., Meng, X.-Y., & Kang, J. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02890-3
- Authors
- Heldt, S. A., & Ressler, K. J.
- Affiliations
- Emory University (US)
- Howard Hughes Medical Institute (US)
- ORCID
- Ressler, Kerry J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-05-26
- Volume
- 30
- Issue
- 21
- Pages
- 7139-7151
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2905594
- OpenAlex
- W2095315913
- Cited by
- 42
- References
- 84
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 1 · 2018: 5 · 2017: 5 · 2016: 4 · 2015: 2 · 2014: 4 · 2013: 5 · 2012: 3
- FWCI
- 1.29
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Howard Hughes Medical Institute
- Burroughs Wellcome Fund (DA019624, P51RR000165)
- National Institutes of Health
- Yerkes National Primate Research Center, Emory University (P51RR000165)
- National Institute of Mental Health (RC1MH088467, F32MH073389)
- National Institute on Drug Abuse (R01DA019624, DA-019624)
- National Center for Research Resources (P51RR000165)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Psychiatry and Mental health › Epilepsy research and treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- amygdala, benzodiazepines, diazepam, zolpidem, anticonvulsant activity, sedation, locomotor inhibition, anxiolysis, GABAA receptor subunits, Cre-loxP system, pharmacogenetics
- MeSH terms
- Zolpidem, Amygdala, Animals, Animals, Newborn, Anticonvulsants, Benzodiazepines, Cell Line, Transformed, Cells, Cultured, Disease Models, Animal, Dose-Response Relationship, Drug, Epilepsy, Exploratory Behavior, Gene Expression Regulation, Hippocampus, Humans, Hypnotics and Sedatives, Locomotion, Male, Mice, Inbred C57BL, Mice, Transgenic, Pentylenetetrazole, Pyridines, Receptors, GABA-A, RNA, Messenger, Anti-Anxiety Agents, Transfection, Maze Learning, Green Fluorescent Proteins, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review