Abstract
Stress is a risk factor for depressive and anxiety disorders. Changes in lifestyle patterns that are associated with increased stress therefore place a greater burden on mental health. Stress challenges the organism’s homeostatic mechanisms, triggering a cascade of events that should, normally, maintain or allow a return to equilibrium. Stressful events are perceived by sensory systems in the brain, facilitating evaluation and comparison of the existing and previous stimuli as well as the activation of hormones responsible for energy mobilization. The limbic system coordinates the release of corticosteroids, the primary stress hormones, by modulating activation of the hypothalamic paraventricular nucleus (PVN). The amygdala, a limbic structure related to emotional behavior, has a putative role in the evaluation of emotional events and formation of fearful memories; it is also a target of the neurochemical and hormonal mediators of stress. Clinical and experimental data have correlated changes in the structure/function of the amygdala with emotional disorders such as anxiety. In this chapter we review the neuroendocrinology of the stress response, focusing on the role of the limbic system in its establishment and supplementing that information with new experimental data that demonstrates the relationship between stress and anxiety disorders; we also discuss the structural changes that occur in the amygdala after stress.
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References
Abercrombie ED, Jacobs BL (1987) Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. I. Acutely presented stressful and nonstressful stimuli. J Neurosci 7(9):2837–2843
Akirav I, Maroun M (2007) The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast 30873
Alheid GF (2003) Extended amygdala and basal forebrain. Ann N Y Acad Sci 985:185–205
Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27(1):1–39
Alonso J, Lepine JP (2007) Overview of key data from the European Study of the Epidemiology of Mental Disorders (ESEMeD). J Clin Psychiatry 68(Suppl 2):3–9
American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders (DSM-IV), 4th edn. American Psychiatric Association, Washington, DC
Anisman H, Matheson K (2005) Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev 29(4–5):525–546
Arborelius L, Owens MJ, Plotsky PM, Nemeroff CB (1999) The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 160(1):1–12
Baker DG, West SA, Nicholson WE, Ekhator NN, Kasckow JW, Hill KK, Bruce AB, Orth DN, Geracioti TD Jr (1999) Serial CSF corticotropin-releasing hormone levels and adrenocortical activity in combat veterans with posttraumatic stress disorder. Am.J.Psychiatry 156:585–588
Bale TL, Contarino A, Smith GW, Chan R, Gold LH, Sawchenko PE et al (2000) Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nat Genet 24(4):410–414
Bekker MH, van Mens-Verhulst J (2007) Anxiety disorders: sex differences in prevalence, degree, and background, but gender-neutral treatment. Gend Med 4(Suppl B):S178–S193
Bessa JM, Oliveira M, Cerqueira JJ, Almeida OF, Sousa N (2005) Age-related qualitative shift in emotional behaviour: paradoxical findings after re-exposure of rats in the elevated-plus maze. Behav Brain Res 162(1):135–142
Bishop SJ (2007) Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn Sci 11(7):307–316
Bourin M, Petit-Demouliere B, Dhonnchadha BN, Hascoet M (2007) Animal models of anxiety in mice. Fundam Clin Pharmacol 21(6):567–574
Boyle MP, Kolber BJ, Vogt SK, Wozniak DF, Muglia LJ (2006) Forebrain glucocorticoid receptors modulate anxiety-associated locomotor activation and adrenal responsiveness. J Neurosci 26(7):1971–1978
Bremner JD, Licinio J, Darnell A, Krystal JH, Owens MJ, Southwick SM, Nemeroff CB, Charney DS (1997) Elevated CSF corticotropin-releasing factor concentrations in posttraumatic stress disorder. Am J Psychiatry 154:624–629
Brown JS, Kalish HI, Farber IE (1951) Conditioned fear as revealed by magnitude of startle response to an auditory stimulus. J Exp Psychol 41(5):317–328
Bucy PC, Kluver H (1955) An anatomical investigation of the temporal lobe in the monkey (Macaca mulatta). J Comp Neurol 103(2):151–251
Burdach K (1819–1822) Vom baue und leben des gehirns und röckenmarks, Dyk, Leipzig
Canteras NS, Swanson LW (1992) Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J Comp Neurol 324(2):180–194
Carpenter LL, Carvalho JP, Tyrka AR, Wier LM, Mello AF, Mello MF, Anderson GM, Wilkinson CW, Price LH (2007) Decreased adrenocorticotropic hormone and cortisol responses to stress in healthy adults reporting significant childhood maltreatment. Biol Psychiatry 62(10):1080–1087
Cerqueira JJ, Catania C, Sotiropoulos I, Schubert M, Kalisch R, Almeida OF et al (2005a) Corticosteroid status influences the volume of the rat cingulate cortex - a magnetic resonance imaging study. J Psychiatr Res 39(5):451–460
Cerqueira JJ, Pego JM, Taipa R, Bessa JM, Almeida OF, Sousa N (2005b) Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 25(34):7792–7800
Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007a) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27(11):2781–2787
Cerqueira JJ, Taipa R, Uylings HB, Almeida OF, Sousa N (2007b) Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb Cortex 17(9):1998–2006
Cerqueira JJ, Almeida OF, Sousa N (2008) The stressed prefrontal cortex. Left? Right!. Brain Behav Immun 22(5):630–638
Chalmers DT, Lovenberg TW, De Souza EB (1995) Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J Neurosci 15(10):6340–6350
Chan RK, Brown ER, Ericsson A, Kovacs KJ, Sawchenko PE (1993) A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry. J Neurosci 13(12):5126–5138
Charney DS, Deutch AY, Krystal JH, Southwick SW, Davis M (1993) Psychobiologic mechanisms of posttraumatic stress disorder. Arch Gen Psychiatry 50(4):295–305
Chen R, Lewis KA, Perrin MH, Vale WW (1993) Expression cloning of a human corticotropin-releasing-factor receptor. Proc Natl Acad Sci USA 90(19):8967–8971
Choi DC, Furay AR, Evanson NK, Ostrander MM, Ulrich-Lai YM, Herman JP (2007) Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 27(8):2025–2034
Chrousos GP, Kino T (2007) Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress 10(2):213–219
Cole RL, Sawchenko PE (2002) Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 22(3):959–969
Coste SC, Kesterson RA, Heldwein KA, Stevens SL, Heard AD, Hollis JH et al (2000) Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat Genet 24(4):403–409
Cullinan WE, Herman JP, Watson SJ (1993) Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 332(1):1–20
Cullinan WE, Herman JP, Battaglia DF, Akil H, Watson SJ (1995) Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64(2):477–505
Dagnino-Subiabre A, Terreros G, Carmona-Fontaine C, Zepeda R, Orellana JA, Diaz-Veliz G et al (2005) Chronic stress impairs acoustic conditioning more than visual conditioning in rats: morphological and behavioural evidence. Neuroscience 135(4):1067–1074
Dautzenberg FM, Hauger RL (2002) The CRF peptide family and their receptors: yet more partners discovered. Trends Pharmacol Sci 23(2):71–77
Davies DC, Martinez-Garcia F, Lanuza E, Novejarque A (2002) Striato-amygdaloid transition area lesions reduce the duration of tonic immobility in the lizard Podarcis hispanica. Brain Res Bull 57(3–4):537–541
Davis M (1986) Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm. Behav Neurosci 100(6):814–824
Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375
Davis M (1998) Are different parts of the extended amygdala involved in fear versus anxiety? Biol Psychiatry 44(12):1239–1247
Davis M (2006) Neural systems involved in fear and anxiety measured with fear-potentiated startle. Am Psychol 61(8):741–756
Davis M, Walker DL, Lee Y (1997) Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos Trans R Soc Lond B Biol Sci 352(1362):1675–1687
de Kloet ER, Joels M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6(6):463–475
De Olmos JS, Beltramino CA, Alheid G (2004) Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical and chemoarchitectonical survey. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier, Amsterdam
Dong HW, Swanson LW (2004) Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J Comp Neurol 468(2):277–298
Dong HW, Swanson LW (2006a) Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol 494(1):142–178
Dong HW, Swanson LW (2006b) Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J Comp Neurol 494(1):75–107
Dong HW, Swanson LW (2006c) Projections from bed nuclei of the stria terminalis, magnocellular nucleus: implications for cerebral hemisphere regulation of micturition, defecation, and penile erection. J Comp Neurol 494(1):108–141
Dong HW, Petrovich GD, Swanson LW (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res Brain Res Rev 38(1–2):192–246
Dranovsky A, Hen R (2006) Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 59(12):1136–1143
Dunn JD (1987) Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis. Brain Res 407(2):327–331
Dunn AJ, File SE (1987) Corticotropin-releasing factor has an anxiogenic action in the social interaction test. Horm Behav 21(2):193–202
Duvarci S, Pare D (2007) Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 27(16):4482–4491
Eisenberg M, Dudai Y (2004) Reconsolidation of fresh, remote, and extinguished fear memory in Medaka: old fears don’t die. Eur J Neurosci 20(12):3397–3403
Espejo EP, Hammen CL, Connolly NP, Brennan PA, Najman JM, Bor W (2007) Stress sensitization and adolescent depressive severity as a function of childhood adversity: a link to anxiety disorders. J Abnorm Child Psychol 35(2):287–299
Feldman S, Conforti N, Melamed E (1987) Paraventricular nucleus serotonin mediates neurally stimulated adrenocortical secretion. Brain Res Bull 18(2):165–168
Figueiredo HF, Bodie BL, Tauchi M, Dolgas CM, Herman JP (2003) Stress integration after acute and chronic predator stress: differential activation of central stress circuitry and sensitization of the hypothalamo-pituitary-adrenocortical axis. Endocrinology 144(12):5249–5258
File SE (1996) Recent developments in anxiety, stress, and depression. Pharmacol Biochem Behav 54(1):3–12
File SE, Johnston AL, Baldwin HA (1988) Anxiolytic and anxiogenic drugs: changes in behaviour and endocrine responses. Stress Med 4(4):221–230
Fuchs E, Fliugge G (2006) Experimental animal models for the simulation of depression and anxiety. Dialogues Clin Neurosci 8(3):323–333
Gann DS, Ward DG, Baertschi AJ, Carlson DE, Maran JW (1977) Neural control of ACTH release in response to hemorrhage. Ann N Y Acad Sci 297:477–497
Gewirtz JC, McNish KA, Davis M (1998) Lesions of the bed nucleus of the stria terminalis block sensitization of the acoustic startle reflex produced by repeated stress, but not fear-potentiated startle. Prog Neuropsychopharmacol Biol Psychiatry 22(4):625–648
Gliner JA (1972) Predictable vs. unpredictable shock: preference behavior and stomach ulceration. Physiol Behav 9(5):693–698
Goddard GV (1964) Functions of the amygdala. Psychol Bull 62:89–109
Greaves-Lord K, Ferdinand RF, Oldehinkel AJ, Sondeijker FE, Ormel J, Verhulst FC (2007) Higher cortisol awakening response in young adolescents with persistent anxiety problems. Acta Psychiatr Scand 116(2):137–144
Gum AM, Cheavens JS (2008) Psychiatric comorbidity and depression in older adults. Curr Psychiatry Rep 10(1):23–29
Heinrichs SC, Koob GF (2004) Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J Pharmacol Exp Ther 311(2):427–440
Heinrichs SC, Lapsansky J, Lovenberg TW, De Souza EB, Chalmers DT (1997) Corticotropin-releasing factor CRF1, but not CRF2, receptors mediate anxiogenic-like behavior. Regul Pept 71(1):15–21
Hammen C (2005) Stress and Depression. Annu Rev Clin Psychol 1:293–319
Herman JP, Cullinan WE, Watson SJ (1994) Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J Neuroendocrinol 6(4):433–442
Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20(2):78–84
Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC et al (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24(3):151–180
Herman JP, Ostrander MM, Mueller NK, Figueiredo H (2005) Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 29(8):1201–1213
Hermann B, Landgraf R, Keck ME, Wigger A, Morrow AL, Strohle A (2000) Pharmacological characterisation of cortical gamma-aminobutyric acid type A (GABAA) receptors in two Wistar rat lines selectively bred for high and low anxiety-related behaviour. World J Biol Psychiatry 1(3):137–143
Hettema JM, Neale MC, Kendler KS (2001) A review and meta-analysis of the genetic epidemiology of anxiety disorders. Am J Psychiatry 158(10):1568–1578
Hettema JM, Prescott CA, Myers JM, Neale MC, Kendler KS (2005) The structure of genetic and environmental risk factors for anxiety disorders in men and women. Arch Gen Psychiatry 62(2):182–189
Imhof JT, Coelho ZM, Schmitt ML, Morato GS, Carobrez AP (1993) Influence of gender and age on performance of rats in the elevated plus maze apparatus. Behav Brain Res 56(2):177–180
Johnston JB (1923) Further contributions to the study of the evolution of the forebrain. J Comp Neurol 35(5):337–481
Ju G, Swanson LW (1989) Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: I. Cytoarchitecture. J Comp Neurol 280(4):587–602
Ju G, Swanson LW, Simerly RB (1989) Studies on the cellular architecture of the bed nuclei of the stria terminalis in the rat: II. Chemoarchitecture. J Comp Neurol 280(4):603–621
Keck ME, Sartori SB, Welt T, Muller MB, Ohl F, Holsboer F et al (2005) Differences in serotonergic neurotransmission between rats displaying high or low anxiety/depression-like behaviour: effects of chronic paroxetine treatment. J Neurochem 92(5):1170–1179
Kessler MS, Murgatroyd C, Bunck M, Czibere L, Frank E, Jacob W et al (2007a) Diabetes insipidus and, partially, low anxiety-related behaviour are linked to a SNP-associated vasopressin deficit in LAB mice. Eur J Neurosci 26(10):2857–2864
Kessler RC, Amminger GP, Aguilar-Gaxiola S, Alonso J, Lee S, Ustun TB (2007b) Age of onset of mental disorders: a review of recent literature. Curr Opin Psychiatry 20(4):359–364
Koch M (1999) The neurobiology of startle. Prog Neurobiol 59(2):107–128
Lancel M, Muller-Preuss P, Wigger A, Landgraf R, Holsboer F (2002) The CRH1 receptor antagonist R121919 attenuates stress-elicited sleep disturbances in rats, particularly in those with high innate anxiety. J Psychiatr Res 36(4):197–208
Lau SH, Rivier J, Vale W, Kaiser ET, Kezdy FJ (1983) Surface properties of an amphiphilic peptide hormone and of its analog: corticotropin-releasing factor and sauvagine. Proc Natl Acad Sci USA 80(23):7070–7074
LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184
LeDoux J (2007) The amygdala. Curr Biol 17(20):R868–R874
Lee Y, Davis M (1997a) Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J Neurosci 17(16):6434–6446
Lee Y, Davis M (1997b) Role of the septum in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J Neurosci 17(16):6424–6433
Lee Y, Schulkin J, Davis M (1994) Effect of corticosterone on the enhancement of the acoustic startle reflex by corticotropin releasing factor (CRF). Brain Res 666(1):93–98
Lenze EJ, Wetherell JL (2009) Bringing the bedside to the bench, and then to the community: a prospectus for intervention research in late-life anxiety disorders. Int J Geriatr Psychiatry 24(1):1–14
Liberzon I, Lopez JF, Flagel SB, Vazquez DM, Young EA (1999) Differential regulation of hippocampal glucocorticoid receptors mRNA and fast feedback: relevance to post-traumatic stress disorder. J Neuroendocrinol 11(1):11–17
Liebsch G, Landgraf R, Gerstberger R, Probst JC, Wotjak CT, Engelmann M et al (1995) Chronic infusion of a CRH1 receptor antisense oligodeoxynucleotide into the central nucleus of the amygdala reduced anxiety-related behavior in socially defeated rats. Regul Pept 59(2):229–239
Liebsch G, Linthorst AC, Neumann ID, Reul JM, Holsboer F, Landgraf R (1998a) Behavioral, physiological, and neuroendocrine stress responses and differential sensitivity to diazepam in two Wistar rat lines selectively bred for high- and low-anxiety-related behavior. Neuropsychopharmacology 19(5):381–396
Liebsch G, Montkowski A, Holsboer F, Landgraf R (1998b) Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour. Behav Brain Res 94(2):301–310
Liebsch G, Landgraf R, Engelmann M, Lorscher P, Holsboer F (1999) Differential behavioural effects of chronic infusion of CRH 1 and CRH 2 receptor antisense oligonucleotides into the rat brain. J Psychiatr Res 33(2):153–163
Lister RG (1990) Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46(3):321–340
Lovenberg TW, Liaw CW, Grigoriadis DE, Clevenger W, Chalmers DT, De Souza EB et al (1995) Cloning and characterization of a functionally distinct corticotropin-releasing factor receptor subtype from rat brain. Proc Natl Acad Sci USA 92(3):836–840
Maier SF, Amat J, Baratta MV, Paul E, Watkins LR (2006) Behavioral control, the medial prefrontal cortex, and resilience. Dialogues Clin Neurosci 8(4):397–406
Mathew SJ, Price RB, Charney DS (2008) Recent advances in the neurobiology of anxiety disorders: implications for novel therapeutics. Am J Med Genet C Semin Med Genet 148(2):89–98
Mayer EA, Fanselow MS (2003) Dissecting the components of the central response to stress. Nat Neurosci 6(10):1011–1012
McEwen BS (2003) Mood disorders and allostatic load. Biol Psychiatry 54(3):200–207
McEwen BS (2004) Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann N Y Acad Sci 1032:1–7
McEwen BS (2005) Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 54(5 Suppl 1):20–23
McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87(3):873–904
McLaughlin KJ, Gomez JL, Baran SE, Conrad CD (2007) The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 1161:56–64
Merikangas KR, Kalaydjian A (2007) Magnitude and impact of comorbidity of mental disorders from epidemiologic surveys. Curr Opin Psychiatry 20(4):353–358
Mesquita AR, Pego JM, Summavielle T, Maciel P, Almeida OF, Sousa N (2007) Neurodevelopment milestone abnormalities in rats exposed to stress in early life. Neuroscience 147(4):1022–1033
Miracle AD, Brace MF, Huyck KD, Singler SA, Wellman CL (2006) Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 85(3):213–218
Mitev YA, Darwish M, Wolf SS, Holsboer F, Almeida OF, Patchev VK (2003) Gender differences in the regulation of 3 alpha-hydroxysteroid dehydrogenase in rat brain and sensitivity to neurosteroid-mediated stress protection. Neuroscience 120(2):541–549
Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S (2005) Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA 102(26):9371–9376
Mizoguchi K, Ishige A, Aburada M, Tabira T (2003) Chronic stress attenuates glucocorticoid negative feedback: involvement of the prefrontal cortex and hippocampus. Neuroscience 119(3):887–897
Moffitt TE, Caspi A, Harrington H, Milne BJ, Melchior M, Goldberg D, Poulton R (2007) Generalized anxiety disorder and depression: childhood risk factors in a birth cohort followed to age 32. Psychol Med 37(3):441–452
Moussavi S, Chatterji S, Verdes E, Tandon A, Patel V, Ustun B (2007) Depression, chronic diseases, and decrements in health: results from the World Health Surveys. Lancet 370(9590):851–858
Musselman DL, Nemeroff CB (2000) Depression really does hurt your heart: stress, depression, and cardiovascular disease. Prog Brain Res 122:43–59
Nakamori T, Morimoto A, Murakami N (1993) Effect of a central CRF antagonist on cardiovascular and thermoregulatory responses induced by stress or IL-1 beta. Am J Physiol 265(4 Pt 2):R834–R839
Neumann ID, Wigger A, Liebsch G, Holsboer F, Landgraf R (1998) Increased basal activity of the hypothalamo-pituitary-adrenal axis during pregnancy in rats bred for high anxiety-related behaviour. Psychoneuroendocrinology 23(5):449–463
Pêgo JM, Morgado P, Pinto LG, Cerqueira JJ, Almeida OF, Sousa N (2008) Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur J Neurosci 27(6):1503–1516
Pêgo JM, Morgado P, Cerqueira JJ, Almeida OF, Sousa N (2006) Mismatch between anxiety status and morphometric parameters in the amygdala and bed nucleus of the stria terminalis. Behav Brain Res 173(2):320–325
Petrovich GD, Canteras NS, Swanson LW (2001) Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Brain Res Rev 38(1–2):247–289
Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106(2):274–285
Portavella M, Torres B, Salas C, Papini MR (2004) Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus). Neurosci Lett 362(2):75–78
Prewitt CM, Herman JP (1998) Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J Chem Neuroanat 15(3):173–185
Radulovic J, Ruhmann A, Liepold T, Spiess J (1999) Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19(12):5016–5025
Reul JM, de Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117(6):2505–2511
Reul JM, de Kloet ER (1986) Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis. J Steroid Biochem 24(1):269–272
Reul JM, Holsboer F (2002) Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr Opin Pharmacol 2(1):23–33
Risbrough VB, Stein MB (2006) Role of corticotropin releasing factor in anxiety disorders: a translational research perspective. Horm Behav 50(4):550–561
Robinson E (1963) Effect of Amygdalectomy on Fear-Motivated Behavior in Rats. J Comp Physiol Psychol 56:814–820
Rosen JB, Fanselow MS, Young SL, Sitcoske M, Maren S (1998) Immediate-early gene expression in the amygdala following footshock stress and contextual fear conditioning. Brain Res 796(1–2):132–142
Rubinow MJ, Drogos LL, Juraska JM (2007) Age-related dendritic hypertrophy and sexual dimorphism in rat basolateral amygdala. Neurobiol Aging 30(1):137–146
Sapolsky RM (1999) Glucocorticoids, stress, and their adverse neurological effects: relevance to aging. Exp Gerontol 34(6):721–732
Sapolsky RM (2000) Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 57(10):925–935
Sapolsky RM, Krey LC, McEwen BS (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 7(3):284–301
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89
Sawchenko PE, Swanson LW, Steinbusch HW, Verhofstad AA (1983) The distribution and cells of origin of serotonergic inputs to the paraventricular and supraoptic nuclei of the rat. Brain Res 277(2):355–360
Shekhar A, McCann UD, Meaney MJ, Blanchard DC, Davis M, Frey KA et al (2001) Summary of a National Institute of Mental Health workshop: developing animal models of anxiety disorders. Psychopharmacology (Berl) 157(4):327–339
Shelton RC (2007) The molecular neurobiology of depression. Psychiatr Clin North Am 30(1):1–11
Sibille E, Pavlides C, Benke D, Toth M (2000) Genetic inactivation of the Serotonin(1A) receptor in mice results in downregulation of major GABA(A) receptor alpha subunits, reduction of GABA(A) receptor binding, and benzodiazepine-resistant anxiety. J Neurosci 20(8):2758–2765
Skorzewska A, Bidzinski A, Lehner M, Turzynska D, Wislowska-Stanek A, Sobolewska A et al (2006) The effects of acute and chronic administration of corticosterone on rat behavior in two models of fear responses, plasma corticosterone concentration, and c-Fos expression in the brain structures. Pharmacol Biochem Behav 85(3):522–534
Skutella T, Probst JC, Renner U, Holsboer F, Behl C (1998) Corticotropin-releasing hormone receptor (type I) antisense targeting reduces anxiety. Neuroscience 85(3):795–805
Smith MA, Brady LS, Glowa J, Gold PW, Herkenham M (1991) Effects of stress and adrenalectomy on tyrosine hydroxylase mRNA levels in the locus ceruleus by in situ hybridization. Brain Res 544(1):26–32
Sorrells SF, Sapolsky RM (2007) An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21(3):259–272
Sousa N, Almeida OF (2002) Corticosteroids: sculptors of the hippocampal formation. Rev Neurosci 13(1):59–84
Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97(2):253–266
Sousa N, Almeida OF, Wotjak CT (2006) A hitchhiker’s guide to behavioral analysis in laboratory rodents. Genes Brain Behav 5(Suppl 2):5–24
Sousa N, Cerqueira JJ, Almeida OF (2008) Corticosteroid receptors and neuroplasticity. Brain Res Rev 57(2):561–570
Steckler T, Holsboer F (1999) Corticotropin-releasing hormone receptor subtypes and emotion. Biol Psychiatry 46(11):1480–1508
Swanson LW (1998) Brain Maps: Structure of the rat brain, 2nd edn. Elsevier, Amsterdam, p 267
Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21(8):323–331
Swerdlow NR, Geyer MA, Vale WW, Koob GF (1986) Corticotropin-releasing factor potentiates acoustic startle in rats: blockade by chlordiazepoxide. Psychopharmacology (Berl) 88(2):147–152
Valdez GR, Zorrilla EP, Rivier J, Vale WW, Koob GF (2003) Locomotor suppressive and anxiolytic-like effects of urocortin 3, a highly selective type 2 corticotropin-releasing factor agonist. Brain Res 980(2):206–212
Vesga-López O, Schneier FR, Wang S, Heimberg RG, Liu SM, Hasin DS, Blanco C (2008) Gender differences in generalized anxiety disorder: results from the National Epidemiologic Survey on Alcohol and Related Conditions (NESARC). J Clin Psychiatry 69:1606–1616
Vyas A, Chattarji S (2004) Modulation of different states of anxiety-like behavior by chronic stress. Behav Neurosci 118(6):1450–1454
Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22(15):6810–6818
Vyas A, Bernal S, Chattarji S (2003) Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res 965(1–2):290–294
Walker DL, Toufexis DJ, Davis M (2003) Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463(1–3):199–216
Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65(5):427–451
Weiskrantz L (1956) Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J Comp Physiol Psychol 49(4):381–391
Whitnall MH (1993) Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Prog Neurobiol 40(5):573–629
Wigger A, Loerscher P, Weissenbacher P, Holsboer F, Landgraf R (2001) Cross-fostering and cross-breeding of HAB and LAB rats: a genetic rat model of anxiety. Behav Genet 31(4):371–382
Yang YL, Chao PK, Ro LS, Wo YY, Lu KT (2007) Glutamate NMDA receptors within the amygdala participate in the modulatory effect of glucocorticoids on extinction of conditioned fear in rats. Neuropsychopharmacology 32(5):1042–1051
Zhao Y, Valdez GR, Fekete EM, Rivier JE, Vale WW, Rice KC, Weiss F, Zorrilla EP (2007) Subtype-selective corticotropin-releasing factor receptor agonists exert contrasting, but not opposite, effects on anxiety-related behavior in rats. J Pharmacol Exp Ther 323:846–854
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Pêgo, J.M., Sousa, J.C., Almeida, O., Sousa, N. (2009). Stress and the Neuroendocrinology of Anxiety Disorders. In: Stein, M., Steckler, T. (eds) Behavioral Neurobiology of Anxiety and Its Treatment. Current Topics in Behavioral Neurosciences, vol 2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7854_2009_13
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