Cited by 56Stress Responses and CortisolNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

Long-Term Behavioral Programming Induced by Peripuberty Stress in Rats Is Accompanied by GABAergic-Related Alterations in the Amygdala

Open access
Tzanoulinou, Stamatina, García-Mompó, Clara, Castillo-Gómez, Esther, Veenit, Vandana, Nacher, Juan, Sandi, Carmen·2014·PLoS ONE

Abstract

Stress during childhood and adolescence is a risk factor for psychopathology. Alterations in γ-aminobutyric acid (GABA), the main inhibitory neurotransmitter in the brain, have been found following stress exposure and fear experiences and are often implicated in anxiety and mood disorders. Abnormal amygdala functioning has also been detected following stress exposure and is also implicated in anxiety and social disorders. However, the amygdala is not a unitary structure; it includes several nuclei with different functions and little is known on the potential differences the impact of early life stress may have on this system within different amygdaloid nuclei. We aimed here to evaluate potential regional differences in the expression of GABAergic-related markers across several amygdaloid nuclei in adult rats subjected to a peripuberty stress protocol that leads to enhanced basal amygdala activity and psychopathological behaviors. More specifically, we investigated the protein expression levels of glutamic acid decarboxylase (GAD; the principal synthesizing enzyme of GABA) and of GABA-A receptor subunits α2 and α3. We found reduced GAD and GABA-A α3, but not α2, subunit protein levels throughout all the amygdala nuclei examined (lateral, basolateral, basomedial, medial and central) and increased anxiety-like behaviors and reduced sociability in peripubertally stressed animals. Our results identify an enduring inhibition of the GABAergic system across the amygdala following exposure to early adversity. They also highlight the suitability of the peripuberty stress model to investigate the link between treatments targeting the dysfunctional GABAergic system in specific amygdala nuclei and recovery of specific stress-induced behavioral dysfunctions.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0094666

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.

A few free checks a day · papers already verified open instantly · results are public

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 115 · Cited by 56

Research works printed but not linked: 100

  1. [1]Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49: 1023– 1039. 11430844
  2. [2]Pechtel P, Pizzagalli DA (2011) Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology (Berl) 214: 55– 70. 20865251 PMC3050094
  3. [3]van der Kolk BA (2003) The neurobiology of childhood trauma and abuse. Child Adolesc Psychiatr Clin N Am 12: 293–317, ix. 12725013
  4. [4]Paus T, Keshavan M, Giedd JN (2008) Why do many psychiatric disorders emerge during adolescence? Nat Rev Neurosci 9: 947– 957. 19002191 PMC2762785
  5. [5]Young EA, Abelson JL, Curtis GC, Nesse RM (1997) Childhood adversity and vulnerability to mood and anxiety disorders. Depress Anxiety 5: 66– 72. 9262936
  6. [6]Andersen SL, Teicher MH (2008) Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci 31: 183– 191. 18329735
  7. [7]Conti G, Hansman C, Heckman JJ, Novak MF, Ruggiero A, et al (2012) Primate evidence on the late health effects of early-life adversity. Proc Natl Acad Sci U S A 109: 8866– 8871. 22615410 PMC3384158
  8. [8]Corcoran CA, Pierre PJ, Haddad T, Bice C, Suomi SJ, et al (2012) Long-term effects of differential early rearing in rhesus macaques: behavioral reactivity in adulthood. Dev Psychobiol 54: 546– 555. 22072233 PMC3298575
  9. [9]Marquez C, Poirier GL, Cordero MI, Larsen MH, Groner A, et al (2013) Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Transl Psychiatry 3: e216. 23321813 PMC3566724
  10. [11]Jacobson-Pick S, Richter-Levin G (2010) Differential impact of juvenile stress and corticosterone in juvenility and in adulthood, in male and female rats. Behav Brain Res 214: 268– 276. 20561965
  11. [15]Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, et al (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223: 403– 410. 21536077 PMC3119771
  12. [16]Hariri AR, Whalen PJ (2011) The amygdala: inside and out. F1000 Biol Rep 3: 2. 21399763 PMC3042316
  13. [17]Sandi C, Richter-Levin G (2009) From high anxiety trait to depression: a neurocognitive hypothesis. Trends Neurosci 32: 312– 320. 19409624
  14. [18]Miskovic V, Schmidt LA (2012) Social fearfulness in the human brain. Neurosci Biobehav Rev 36: 459– 478. 21855571
  15. [20]Vermetten E, Schmahl C, Southwick SM, Bremner JD (2007) Positron tomographic emission study of olfactory induced emotional recall in veterans with and without combat-related posttraumatic stress disorder. Psychopharmacol Bull 40: 8– 30. 17285093 PMC3236699
  16. [21]Driessen M, Beblo T, Mertens M, Piefke M, Rullkoetter N, et al (2004) Posttraumatic stress disorder and fMRI activation patterns of traumatic memory in patients with borderline personality disorder. Biol Psychiatry 55: 603– 611. 15013829
  17. [23]Chung YA, Kim SH, Chung SK, Chae JH, Yang DW, et al (2006) Alterations in cerebral perfusion in posttraumatic stress disorder patients without re-exposure to accident-related stimuli. Clin Neurophysiol 117: 637– 642. 16426890
  18. [24]Bryant RA, Felmingham KL, Kemp AH, Barton M, Peduto AS, et al (2005) Neural networks of information processing in posttraumatic stress disorder: a functional magnetic resonance imaging study. Biol Psychiatry 58: 111– 118. 16038681
  19. [25]Shin LM, Shin PS, Heckers S, Krangel TS, Macklin ML, et al (2004) Hippocampal function in posttraumatic stress disorder. Hippocampus 14: 292– 300. 15132428
  20. [26]Nemeroff CB (2003) The role of GABA in the pathophysiology and treatment of anxiety disorders. Psychopharmacol Bull 37: 133– 146. 15131523
  21. [27]Lydiard RB (2003) The role of GABA in anxiety disorders. J Clin Psychiatry 64 Suppl 3 21– 27. 12662130
  22. [28]Hettema JM, Kettenmann B, Ahluwalia V, McCarthy C, Kates WR, et al (2012) Pilot multimodal twin imaging study of generalized anxiety disorder. Depress Anxiety 29: 202– 209. 21994092 PMC3258467
  23. [29]Geuze E, van Berckel BN, Lammertsma AA, Boellaard R, de Kloet CS, et al. (2008) Reduced GABAA benzodiazepine receptor binding in veterans with post-traumatic stress disorder. Mol Psychiatry 13: 74–83, 73. 17667960
  24. [30]Lindefors N (1993) Dopaminergic regulation of glutamic acid decarboxylase mRNA expression and GABA release in the striatum: a review. Prog Neuropsychopharmacol Biol Psychiatry 17: 887– 903. 8278600
  25. [31]Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7: 91– 100. 2069816
  26. [32]Soghomonian JJ, Martin DL (1998) Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 19: 500– 505. 9871412
  27. [33]Fatemi SH, Halt AR, Stary JM, Kanodia R, Schulz SC, et al (2002) Glutamic acid decarboxylase 65 and 67 kDa proteins are reduced in autistic parietal and cerebellar cortices. Biol Psychiatry 52: 805– 810. 12372652
  28. [34]Fatemi SH, Stary JM, Earle JA, Araghi-Niknam M, Eagan E (2005) GABAergic dysfunction in schizophrenia and mood disorders as reflected by decreased levels of glutamic acid decarboxylase 65 and 67 kDa and Reelin proteins in cerebellum. Schizophr Res 72: 109– 122. 15560956
  29. [35]Sibille E, Morris HM, Kota RS, Lewis DA (2011) GABA-related transcripts in the dorsolateral prefrontal cortex in mood disorders. Int J Neuropsychopharmacol 14: 721– 734. 21226980 PMC3388740
  30. [36]Smith KS, Engin E, Meloni EG, Rudolph U (2012) Benzodiazepine-induced anxiolysis and reduction of conditioned fear are mediated by distinct GABAA receptor subtypes in mice. Neuropharmacology 63: 250– 258. 22465203 PMC3372637
  31. [37]Smith KS, Meloni EG, Myers KM, Van’t Veer A, Carlezon WA Jr, et al (2011) Reduction of fear-potentiated startle by benzodiazepines in C57BL/6J mice. Psychopharmacology (Berl) 213: 697– 706. 20922362 PMC3056161
  32. [38]Cole BJ, Hillmann M, Seidelmann D, Klewer M, Jones GH (1995) Effects of benzodiazepine receptor partial inverse agonists in the elevated plus maze test of anxiety in the rat. Psychopharmacology (Berl) 121: 118– 126. 8539336
  33. [39]Albrechet-Souza L, Borelli KG, Carvalho MC, Brandao ML (2009) The anterior cingulate cortex is a target structure for the anxiolytic-like effects of benzodiazepines assessed by repeated exposure to the elevated plus maze and Fos immunoreactivity. Neuroscience 164: 387– 397. 19699782
  34. [40]Anderson NJ, Daunais JB, Friedman DP, Grant KA, McCool BA (2007) Long-term ethanol self-administration by the nonhuman primate, Macaca fascicularis, decreases the benzodiazepine sensitivity of amygdala GABA(A) receptors. Alcohol Clin Exp Res 31: 1061– 1070. 17428292 PMC2288551
  35. [41]Paulus MP, Feinstein JS, Castillo G, Simmons AN, Stein MB (2005) Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. Arch Gen Psychiatry 62: 282– 288. 15753241
  36. [42]Barbalho CA, Nunes-de-Souza RL, Canto-de-Souza A (2009) Similar anxiolytic-like effects following intra-amygdala infusions of benzodiazepine receptor agonist and antagonist: evidence for the release of an endogenous benzodiazepine inverse agonist in mice exposed to elevated plus-maze test. Brain Res 1267: 65– 76. 19268657
  37. [43]Sanders SK, Shekhar A (1995) Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav 52: 701– 706. 8587908
  38. [44]Sanders SK, Shekhar A (1991) Blockade of GABAA receptors in the region of the anterior basolateral amygdala of rats elicits increases in heart rate and blood pressure. Brain Res 567: 101– 110. 1667743
  39. [45]Jacobson-Pick S, Richter-Levin G (2012) Short- and long-term effects of juvenile stressor exposure on the expression of GABAA receptor subunits in rats. Stress 15: 416– 424. 22044189
  40. [46]Jacobson-Pick S, Elkobi A, Vander S, Rosenblum K, Richter-Levin G (2008) Juvenile stress-induced alteration of maturation of the GABAA receptor alpha subunit in the rat. Int J Neuropsychopharmacol 11: 891– 903. 18364065
  41. [47]Mohler H (2012) The GABA system in anxiety and depression and its therapeutic potential. Neuropharmacology 62: 42– 53. 21889518
  42. [48]Malizia AL, Cunningham VJ, Bell CJ, Liddle PF, Jones T, et al (1998) Decreased brain GABA(A)-benzodiazepine receptor binding in panic disorder: preliminary results from a quantitative PET study. Arch Gen Psychiatry 55: 715– 720. 9707382
  43. [50]Bremner JD, Innis RB, Southwick SM, Staib L, Zoghbi S, et al (2000) Decreased benzodiazepine receptor binding in prefrontal cortex in combat-related posttraumatic stress disorder. Am J Psychiatry 157: 1120– 1126. 10873921
  44. [51]Nutt DJ, Malizia AL (2004) Structural and functional brain changes in posttraumatic stress disorder. J Clin Psychiatry 65 Suppl 1 11– 17. 14728092
  45. [52]Fritschy JM, Mohler H (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359: 154– 194. 8557845
  46. [53]Rudolph U, Mohler H (2006) GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr Opin Pharmacol 6: 18– 23. 16376150
  47. [54]Skolnick P (2012) Anxioselective anxiolytics: on a quest for the Holy Grail. Trends Pharmacol Sci 33: 611– 620. 22981367 PMC3482271
  48. [55]Mohler H, Benke D, Benson J, Luscher B, Fritschy JM (1995) GABAA-receptor subtypes in vivo: cellular localization, pharmacology and regulation. Adv Biochem Psychopharmacol 48: 41– 56. 7653325
  49. [56]Mohler H, Knoflach F, Paysan J, Motejlek K, Benke D, et al (1995) Heterogeneity of GABAA-receptors: cell-specific expression, pharmacology, and regulation. Neurochem Res 20: 631– 636. 7643969
  50. [57]Rudolph U, Crestani F, Mohler H (2001) GABA(A) receptor subtypes: dissecting their pharmacological functions. Trends Pharmacol Sci 22: 188– 194. 11282419
  51. [61]Pellow S, File SE (1986) Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24: 525– 529. 2871560
  52. [62]Veenit V, Cordero MI, Tzanoulinou S, Sandi C (2013) Increased corticosterone in peripubertal rats leads to long-lasting alterations in social exploration and aggression. Front Behav Neurosci 7: 26. 23576965 PMC3616252
  53. [64]Kohl C, Riccio O, Grosse J, Zanoletti O, Fournier C, et al (2013) Hippocampal neuroligin-2 overexpression leads to reduced aggression and inhibited novelty reactivity in rats. PLoS One 8: e56871. 23451101 PMC3579928
  54. [65]Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577– 580. 6166661
  55. [66]Varea E, Castillo-Gomez E, Gomez-Climent MA, Blasco-Ibanez JM, Crespo C, et al (2007) Chronic antidepressant treatment induces contrasting patterns of synaptophysin and PSA-NCAM expression in different regions of the adult rat telencephalon. Eur Neuropsychopharmacol 17: 546– 557. 17307340
  56. [67]Marti O, Marti J, Armario A (1994) Effects of chronic stress on food intake in rats: influence of stressor intensity and duration of daily exposure. Physiol Behav 55: 747– 753. 8190805
  57. [69]Bisaz R, Schachner M, Sandi C (2011) Causal evidence for the involvement of the neural cell adhesion molecule, NCAM, in chronic stress-induced cognitive impairments. Hippocampus 21: 56– 71. 19921700
  58. [70]Spruijt BM, van Hooff JA, Gispen WH (1992) Ethology and neurobiology of grooming behavior. Physiol Rev 72: 825– 852. 1320764
  59. [71]van Erp AM, Kruk MR, Meelis W, Willekens-Bramer DC (1994) Effect of environmental stressors on time course, variability and form of self-grooming in the rat: handling, social contact, defeat, novelty, restraint and fur moistening. Behav Brain Res 65: 47– 55. 7880454
  60. [72]Moody TW, Merali Z, Crawley JN (1988) The effects of anxiolytics and other agents on rat grooming behavior. Ann N Y Acad Sci 525: 281– 290. 2455462
  61. [73]Avital A, Ram E, Maayan R, Weizman A, Richter-Levin G (2006) Effects of early-life stress on behavior and neurosteroid levels in the rat hypothalamus and entorhinal cortex. Brain Res Bull 68: 419– 424. 16459196
  62. [74]Bazak N, Kozlovsky N, Kaplan Z, Matar M, Golan H, et al (2009) Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology 34: 844– 858. 19181453
  63. [75]Ilin Y, Richter-Levin G (2009) Enriched environment experience overcomes learning deficits and depressive-like behavior induced by juvenile stress. PLoS One 4: e4329. 19180243 PMC2631645
  64. [76]McCormick CM, Smith C, Mathews IZ (2008) Effects of chronic social stress in adolescence on anxiety and neuroendocrine response to mild stress in male and female rats. Behav Brain Res 187: 228– 238. 17945360
  65. [77]Ito H, Nagano M, Suzuki H, Murakoshi T (2010) Chronic stress enhances synaptic plasticity due to disinhibition in the anterior cingulate cortex and induces hyper-locomotion in mice. Neuropharmacology 58: 746– 757. 20035774
  66. [78]Vidal J, Bie J, Granneman RA, Wallinga AE, Koolhaas JM, et al (2007) Social stress during adolescence in Wistar rats induces social anxiety in adulthood without affecting brain monoaminergic content and activity. Physiol Behav 92: 824– 830. 17651767
  67. [79]Ackermann RF, Finch DM, Babb TL, Engel J Jr (1984) Increased glucose metabolism during long-duration recurrent inhibition of hippocampal pyramidal cells. J Neurosci 4: 251– 264. 6693941 PMC6564752
  68. [80]Nudo RJ, Masterton RB (1986) Stimulation-induced [14C]2-deoxyglucose labeling of synaptic activity in the central auditory system. J Comp Neurol 245: 553– 565. 3009561
  69. [82]Gilabert-Juan J, Castillo-Gomez E, Perez-Rando M, Molto MD, Nacher J (2011) Chronic stress induces changes in the structure of interneurons and in the expression of molecules related to neuronal structural plasticity and inhibitory neurotransmission in the amygdala of adult mice. Exp Neurol 232: 33– 40. 21819983
  70. [83]Phan KL, Fitzgerald DA, Nathan PJ, Tancer ME (2006) Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia. Biol Psychiatry 59: 424– 429. 16256956
  71. [84]Lin HC, Gean PW, Wang CC, Chan YH, Chen PS (2013) The amygdala excitatory/inhibitory balance in a valproate-induced rat autism model. PLoS One 8: e55248. 23383124 PMC3558482
  72. [85]Rubenstein JL, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2: 255– 267. 14606691 PMC6748642
  73. [86]Kash SF, Tecott LH, Hodge C, Baekkeskov S (1999) Increased anxiety and altered responses to anxiolytics in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci U S A 96: 1698– 1703. 9990087 PMC15565
  74. [87]Marowsky A, Fritschy JM, Vogt KE (2004) Functional mapping of GABA A receptor subtypes in the amygdala. Eur J Neurosci 20: 1281– 1289. 15341600
  75. [88]Marowsky A, Rudolph U, Fritschy JM, Arand M (2012) Tonic inhibition in principal cells of the amygdala: a central role for alpha3 subunit-containing GABAA receptors. J Neurosci 32: 8611– 8619. 22723702 PMC6620967
  76. [89]Engin E, Liu J, Rudolph U (2012) alpha2-containing GABA(A) receptors: a target for the development of novel treatment strategies for CNS disorders. Pharmacol Ther 136: 142– 152. 22921455 PMC3478960
  77. [90]Dias R, Sheppard WF, Fradley RL, Garrett EM, Stanley JL, et al (2005) Evidence for a significant role of alpha 3-containing GABAA receptors in mediating the anxiolytic effects of benzodiazepines. J Neurosci 25: 10682– 10688. 16291941 PMC6725841
  78. [91]Atack JR, Hutson PH, Collinson N, Marshall G, Bentley G, et al (2005) Anxiogenic properties of an inverse agonist selective for alpha3 subunit-containing GABA A receptors. Br J Pharmacol 144: 357– 366. 15655523 PMC1576012
  79. [92]Fischer BD, Atack JR, Platt DM, Reynolds DS, Dawson GR, et al (2011) Contribution of GABA(A) receptors containing alpha3 subunits to the therapeutic-related and side effects of benzodiazepine-type drugs in monkeys. Psychopharmacology (Berl) 215: 311– 319. 21190016 PMC3097109
  80. [93]Shiah IS, Yatham LN (1998) GABA function in mood disorders: an update and critical review. Life Sci 63: 1289– 1303. 9768867
  81. [94]Hettema JM, An SS, Neale MC, Bukszar J, van den Oord EJ, et al (2006) Association between glutamic acid decarboxylase genes and anxiety disorders, major depression, and neuroticism. Mol Psychiatry 11: 752– 762. 16718280
  82. [95]Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ (2000) The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22: 219– 229. 10693149
  83. [96]Liu M, Glowa JR (2000) Regulation of benzodiazepine receptor binding and GABA(A) subunit mRNA expression by punishment and acute alprazolam administration. Brain Res 887: 23– 33. 11134586
  84. [97]Bennur S, Shankaranarayana Rao BS, Pawlak R, Strickland S, McEwen BS, et al (2007) Stress-induced spine loss in the medial amygdala is mediated by tissue-plasminogen activator. Neuroscience 144: 8– 16. 17049177
  85. [98]Cordero MI, Poirier GL, Marquez C, Veenit V, Fontana X, et al (2012) Evidence for biological roots in the transgenerational transmission of intimate partner violence. Transl Psychiatry 2: e106. 22832906 PMC3337076
  86. [99]Toledo-Rodriguez M, Sandi C (2007) Stress before puberty exerts a sex- and age-related impact on auditory and contextual fear conditioning in the rat. Neural Plast 2007: 71203. 17671613 PMC1931496
  87. [100]Toledo-Rodriguez M, Pitiot A, Paus T, Sandi C (2012) Stress during puberty boosts metabolic activation associated with fear-extinction learning in hippocampus, basal amygdala and cingulate cortex. Neurobiol Learn Mem 98: 93– 101. 22664720
  88. [101]Haller J, Mikics E, Halasz J, Toth M (2005) Mechanisms differentiating normal from abnormal aggression: glucocorticoids and serotonin. Eur J Pharmacol 526: 89– 100. 16280125
  89. [102]Barad M, Gean PW, Lutz B (2006) The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60: 322– 328. 16919522
  90. [103]Li G, Nair SS, Quirk GJ (2009) A biologically realistic network model of acquisition and extinction of conditioned fear associations in lateral amygdala neurons. J Neurophysiol 101: 1629– 1646. 19036872 PMC2666411
  91. [104]Trezza V, Campolongo P (2009) Toward understanding the neurobiology of social attachment: role of estrogen receptors in the medial amygdala. J Neurosci 29: 1– 2. 19129378 PMC6664922
  92. [105]Veenit V, Riccio O, Sandi C (2014) CRHR1 links peripuberty stress with deficits in social and stress-coping behaviors. J Psychiatr Res. 24630468
  93. [106]Rainnie DG, Bergeron R, Sajdyk TJ, Patil M, Gehlert DR, et al (2004) Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 24: 3471– 3479. 15071094 PMC6729749
  94. [107]Duvarci S, Pare D (2007) Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 27: 4482– 4491. 17442833 PMC6672328
  95. [108]de Kloet ER, de Jong IE, Oitzl MS (2008) Neuropharmacology of glucocorticoids: focus on emotion, cognition and cocaine. Eur J Pharmacol 585: 473– 482. 18417120
  96. [109]Darnaudery M, Maccari S (2008) Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57: 571– 585. 18164765
  97. [110]Cullinan WE, Ziegler DR, Herman JP (2008) Functional role of local GABAergic influences on the HPA axis. Brain Struct Funct 213: 63– 72. 18696110
  98. [111]Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20: 78– 84. 9023876
  99. [112]Martijena ID, Rodriguez Manzanares PA, Lacerra C, Molina VA (2002) Gabaergic modulation of the stress response in frontal cortex and amygdala. Synapse 45: 86– 94. 12112401
  100. [113]Gafford GM, Guo JD, Flandreau EI, Hazra R, Rainnie DG, et al (2012) Cell-type specific deletion of GABA(A)alpha1 in corticotropin-releasing factor-containing neurons enhances anxiety and disrupts fear extinction. Proc Natl Acad Sci U S A 109: 16330– 16335. 22992651 PMC3479581

Authors
Tzanoulinou, S., García-Mompó, C., Castillo-Gómez, E., Veenit, V., Nacher, J., & Sandi, C.
Affiliations
  • École Polytechnique Fédérale de Lausanne (CH)
  • Universitat de València (ES)
Corresponding author
Sandi, Carmen
Venue
PLoS ONE
Published
2014-04-15
Volume
9
Issue
4
Pages
e94666
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2050717527
Cited by
56
References
115
Citations by year
2026: 1 · 2025: 5 · 2024: 2 · 2023: 7 · 2022: 3 · 2021: 3 · 2020: 5 · 2019: 5 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 9 · 2014: 2
FWCI
3.11
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders
  • National Science Foundation
  • École Polytechnique Fédérale de Lausanne (31003AB-135710)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (32512, 135710)
  • Ministerio de Economía y Competitividad (BFU2012-32512)
  • Generalitat Valenciana (PROMETEO2013/069, ACOMP/2012/229)
  • Ministerio de Ciencia e Innovación (BFU2012-32512)
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
early life stress, GABAergic system, amygdala nuclei, glutamic acid decarboxylase, GABAA receptor subunits, anxiety-like behavior, sociability, childhood adversity
MeSH terms
Amygdala, Animals, Anxiety, Behavior, Animal, Body Weight, Exploratory Behavior, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Interpersonal Relations, Puberty, Receptors, GABA-A, Stress, Psychological, Rats, Wistar, Rats

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