Overlapping neurobiology of learned helplessness and conditioned defeat: Implications for PTSD and mood disorders

Hammack, Sayamwong E.; Cooper, Matthew A.; Lezak, Kimberly R.

doi:10.1016/j.neuropharm.2011.02.024

Cited by 142Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsStress Responses and Cortisol

Overlapping neurobiology of learned helplessness and conditioned defeat: Implications for PTSD and mood disorders

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Hammack, Sayamwong E., Cooper, Matthew A., Lezak, Kimberly R.·2012·Neuropharmacology

DOI 10.1016/j.neuropharm.2011.02.024PMC PMC3433056

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Abstract

Exposure to traumatic events can increase the risk for major depressive disorder (MDD) as well as posttraumatic stress disorder (PTSD), and pharmacological treatments for these disorders often involve the modulation of serotonergic (5-HT) systems. Several behavioral paradigms in rodents produce changes in behavior that resemble symptoms of MDD and these behavioral changes are sensitive to antidepressant treatments. Here we review two animal models in which MDD-like behavioral changes are elicited by exposure to an acute traumatic event during adulthood, learned helplessness (LH) and conditioned defeat. In LH, exposure of rats to inescapable, but not escapable, tailshock produces a constellation of behavioral changes that include deficits in fight/flight responding and enhanced anxiety-like behavior. In conditioned defeat, exposure of Syrian hamsters to a social defeat by a more aggressive animal leads to a loss of territorial aggression and an increase in submissive and defensive behaviors in subsequent encounters with non-aggressive conspecifics. Investigations into the neural substrates that control LH and conditioned defeat revealed that increased 5-HT activity in the dorsal raphe nucleus (DRN) is critical for both models. Other key brain regions that regulate the acquisition and/or expression of behavior in these two paradigms include the basolateral amygdala (BLA), central nucleus of the amygdala (CeA) and bed nucleus of the stria terminalis (BNST). In this review, we compare and contrast the role of each of these neural structures in mediating LH and conditioned defeat, and discuss the relevance of these data in developing a better understanding of the mechanisms underlying trauma-related depression. This article is part of a Special Issue entitled 'Post-Traumatic Stress Disorder'.

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The BNST has been implicated in behavioral changes associated with depression; BNST activity has been related to anhedonic behavior after chronic mild stress, and lesions in this structure block the onset of learned helplessness in preclinical models.
“The BNST has also been implicated in behavioral changes associated with depression; in particular, BNST activity has been related to anhedonic behavior after chronic mild stress, whereas lesions in this structure block the onset of learned helplessness in preclinical models [52].”
From The bed nucleus of the stria terminalis as a brain correlate of psychological inflexibility in fibromyalgia (2020) · cites this paper as [52]

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Diagnostic and Statistical Manual of Mental Disorders ( DSM ‐ IV ‐ TR )
Segal, D. L. (2010) · Wiley eBooks · doi:10.1002/9780470479216.corpsy0271 · Cited by 4,683 · see citing works
Learned helplessness: Theory and evidence
Maier, S. F., & Seligman, M. E. (1976) · Journal of Experimental Psychology: General · doi:10.1037/0096-3445.105.1.3 · Cited by 2,494 · see citing works
Molecular Adaptations Underlying Susceptibility and Resistance to Social Defeat in Brain Reward Regions
Krishnan, V., Han, M.-H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., LaPlant, Q., Graham, A., Lutter, M., Lagace, D. C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.09.018 · Cited by 2,307 · cited 2× · see citing works
“…IH -PA Author M anuscript Conditioned Defeat Social defeat is a robust stressor that, like LH, produces an array of behavioral changes including anxiety- and depression-like behavior (Berton et al., 1998; Heinrichs et al., 1992; Keeney et al., 2006; Krishnan et al., 2007; Rodgers and Cole, 1993).”
Background
Pituitary-adrenal and autonomic responses to stress in women after sexual and physical abuse in childhood
Heim, C. (2000) · JAMA · doi:10.1001/jama.284.5.592 · Cited by 1,968 · see citing works
New approaches to antidepressant drug discovery: beyond monoamines
Berton, O., & Nestler, E. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1846 · Cited by 1,589 · see citing works
Hormones, Brain and Behavior
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03789-7 · Cited by 1,543 · see citing works
Elevated Concentrations of CSF Corticotropin-Releasing Factor-Like Immunoreactivity in Depressed Patients
Nemeroff, C. B., Widerlöv, E., Bissette, G., Walléus, H., Karlsson, I., Eklund, K., Kilts, C. D., Loosen, P. T., & Vale, W. (1984) · Science · doi:10.1126/science.6334362 · Cited by 1,485 · see citing works
The role of corticotropin-releasing factor in depression and anxiety disorders
Arborelius, L., Owens, M., Plotsky, P., & Nemeroff, C. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1600001 · Cited by 1,378 · see citing works
Prospective Study of Posttraumatic Stress Disorder and Depression Following Trauma
Shalev, A. Y., Freedman, S., Peri, T., Brandes, D., Sahar, T., Orr, S. P., & Pitman, R. K. (1998) · American Journal of Psychiatry · doi:10.1176/ajp.155.5.630 · Cited by 998 · see citing works
Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus
Amat, J., Baratta, M. V., Paul, E., Bland, S. T., Watkins, L. R., & Maier, S. F. (2005) · Nature Neuroscience · doi:10.1038/nn1399 · Cited by 931 · see citing works
Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression
Chalmers, D., Lovenberg, T. W., & Souza, E. D. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06340.1995 · Cited by 925 · see citing works
Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety
Walker, D. L., Toufexis, D. J., & Davis, M. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01282-2 · Cited by 838 · see citing works
Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor
Ressler, K. J., Mercer, K. B., Bradley, B., Jovanovic, T., Mahan, A., Kerley, K., Norrholm, S. D., Kilaru, V., Smith, A. K., Myers, A. J., et al. (2011) · Nature · doi:10.1038/nature09856 · Cited by 800 · see citing works
Self-citation
Uncontrollability and unpredictability in post-traumatic stress disorder: An animal model.
Foa, E. B., Zinbarg, R., & Rothbaum, B. O. (1992) · Psychological Bulletin · doi:10.1037/0033-2909.112.2.218 · Cited by 787 · see citing works
Stress and Coping
Monat, A. (1991) · Cited by 748 · see citing works
Fear-potentiated startle: A neural and pharmacological analysis
Davis, M., Falls, W. A., Campeau, S., & Kim, M. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90102-v · Cited by 737 · see citing works
Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor.
Maier, S. F., & Watkins, L. R. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.021 · Cited by 737 · see citing works
Animal Model of Depression
McKinney, W. T. (1969) · Archives of General Psychiatry · doi:10.1001/archpsyc.1969.01740200112015 · Cited by 710 · see citing works
The olfactory bulbectomised rat as a model of depression
Song, C., & Leonard, B. E. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.010 · Cited by 700 · see citing works
Cortisol and post-traumatic stress disorder in adults: Systematic review and meta-analysis
Meewisse, M.-L., Reitsma, J. B., De Vries, G.-J., Gersons, B. P. R., & Olff, M. (2007) · British Journal of Psychiatry · doi:10.1192/bjp.bp.106.024877 · Cited by 661 · see citing works
Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems.
Petrovich, G., Canteras, N., & Swanson, L. (2001) · Brain research. Brain research reviews · doi:10.1016/s0165-0173(01)00080-7 · Cited by 628 · see citing works
Role of selective serotonin reuptake inhibitors in psychiatric disorders: a comprehensive review
Vaswani, M., Linda, F. K., & Ramesh, S. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(02)00338-x · Cited by 612 · see citing works
Rethinking the Fear Circuit: The Central Nucleus of the Amygdala Is Required for the Acquisition, Consolidation, and Expression of Pavlovian Fear Conditioning
Wilensky, A. E., Schafe, G. E., Kristensen, M. P., & LeDoux, J. E. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4316-06.2006 · Cited by 533 · see citing works
A role for corticotropin releasing factor and urocortin in behavioral responses to stressors
Koob, G. F., & Heinrichs, S. C. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01991-5 · Cited by 530 · see citing works
Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder
(1993) · American Journal of Psychiatry · doi:10.1176/ajp.150.1.83 · Cited by 517 · see citing works
Importance of studying the contributions of early adverse experience to neurobiological findings in depression
Heim, C., Plotsky, P. M., & Nemeroff, C. B. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300397 · Cited by 514 · see citing works
Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods
Peyron, C., Petit, J.-M., Rampon, C., Jouvet, M., & Luppi, P. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00268-6 · Cited by 509 · see citing works
Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity
Rizvi, T. A., Ennis, M., Behbehani, M. M., & Shipley, M. T. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903030111 · Cited by 500 · see citing works
Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates
Blanchard, D. C., Spencer, R. L., Weiss, S. M., Blanchard, R. J., McEwen, B., & Sakai, R. R. (1995) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)e0045-b · Cited by 475 · see citing works
Recent life events, cortisol, dehydroepiandrosterone and the onset of major depression in high-risk adolescents
Goodyer, I. M., Herbert, J., Tamplin, A., & Altham, P. M. E. (2000) · British Journal of Psychiatry · doi:10.1192/bjp.177.6.499 · Cited by 436 · cited 2× · see citing works
“Exposure to traumatic events, such as those that can produce PTSD, also increase the risk for MDD (Goodyer et al., 2000; Heim et al., 2000; Kohn et al., 2001; Mayou et al., 2001; Shalev et al., 1998); however, risk for MDD might also been linked to a variety of negative life events or adversities that do not meet the…”
Background
Corticotropin-releasing factor immunoreactivity is widely distributed within the central nervous system of the rat: an immunohistochemical study
Cummings, S., Elde, R., Ells, J., & Lindall, A. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-07-01355.1983 · Cited by 414 · see citing works
Serotonin-1A receptor imaging in recurrent depression: replication and literature review
Drevets, W. C., Thase, M. E., Moses-Kolko, E. L., Price, J., Frank, E., Kupfer, D. J., & Mathis, C. (2007) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2007.06.008 · Cited by 399 · see citing works
Bed Nucleus of the Stria Terminalis Subregions Differentially Regulate Hypothalamic–Pituitary–Adrenal Axis Activity: Implications for the Integration of Limbic Inputs
Choi, D. C., Furay, A. R., Evanson, N. K., Ostrander, M. M., Ulrich-Lai, Y. M., & Herman, J. P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4301-06.2007 · Cited by 392 · see citing works
Specificity of the learned helplessness model of depression
Sherman, A. D., Sacquitne, J. L., & Petty, F. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90451-8 · Cited by 391 · see citing works
The Flinders Sensitive Line rat: A selectively bred putative animal model of depression
Overstreet, D. H., Friedman, E. M., Mathé, A. A., & Yadid, G. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.015 · Cited by 375 · see citing works
The organization of divergent axonal projections from the midbrain raphe nuclei in the rat
Imai, H., Steindler, D. A., & Kitai, S. T. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902430307 · Cited by 369 · see citing works
Freewheel Running Prevents Learned Helplessness/Behavioral Depression: Role of Dorsal Raphe Serotonergic Neurons
Greenwood, B. N., Foley, T. E., Day, H. E. W., Campisi, J., Hammack, S. E., Campeau, S., Maier, S. F., & Fleshner, M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02889.2003 · Cited by 367 · see citing works
Self-citation
Reduced Serotonin Type 1AReceptor Binding in Panic Disorder: Figure 1.
Neumeister, A., Bain, E., Nugent, A. C., Carson, R. E., Bonne, O. B., Luckenbaugh, D. A., Eckelman, W. C., Herscovitch, P., Charney, D. S., & Drevets, W. C. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4921-03.2004 · Cited by 352 · see citing works
Untitled work
(1997) · PubMed · Cited by 350 · see citing works
Extended Amygdala and Basal Forebrain
Alheid, G. F. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07082.x · Cited by 334 · see citing works
Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses
Walker, D. L., Miles, L. A., & Davis, M. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.06.022 · Cited by 331 · see citing works
Corticotropin-releasing factor antagonist reduces emotionality in socially defeated rats via direct neurotropic action
Heinrichs, S. C., Pich, E. M., Miczek, K. A., Britton, K. T., & Koob, G. F. (1992) · Brain Research · doi:10.1016/0006-8993(92)90708-h · Cited by 329 · see citing works
Basal cortisol, dexamethasone suppression of cortisol, and MHPG in adolescents after the 1988 earthquake in Armenia
Goenjian, A. K., Yehuda, R., Pynoos, R. S., Steinberg, A. M., Tashjian, M., Yang, R., Najarian, L. M., & Fairbanks, L. A. (1996) · American Journal of Psychiatry · doi:10.1176/ajp.153.7.929 · Cited by 310 · see citing works
Learned helplessness and animal models of depression
Maier, S. F. (1984) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(84)80032-9 · Cited by 309 · see citing works
Effects of Corticotropin-Releasing Factor on Neuronal Activity in the Serotonergic Dorsal Raphe Nucleus
Kirby, L. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00093-7 · Cited by 307 · see citing works
Cortical afferents to the extended amygdala
McDONALD, A. J., SHAMMAH‐LAGNADO, S. J., SHI, C., & DAVIS, M. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09275.x · Cited by 306 · see citing works
Criteria for rationally evaluating animal models of postraumatic stress disorder
Yehuda, R., & Antelman, S. M. (1993) · Biological Psychiatry · doi:10.1016/0006-3223(93)90001-t · Cited by 301 · see citing works
Modulation of anxiety circuits by serotonergic systems
Lowry, C. A., Johnson, P. L., Hay‐Schmidt, A., Mikkelsen, J. D., & Shekhar, A. (2005) · Stress · doi:10.1080/10253890500492787 · Cited by 300 · see citing works
Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor
Grahn, R. E., Will, M. J., Hammack, S. E., Maswood, S., McQueen, M. B., Watkins, L. R., & Maier, S. F. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01208-1 · Cited by 298 · see citing works
Self-citation
Anatomic and functional topography of the dorsal raphe nucleus
ABRAMS, J. K., JOHNSON, P. L., HOLLIS, J. H., & LOWRY, C. A. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.005 · Cited by 284 · see citing works
Differential Effects of Acute and Chronic Social Defeat Stress on Hypothalamic‐Pituitary‐Adrenal Axis Function and Hippocampal Serotonin Release in Mice
Keeney, A. J., Jessop, D. S., Harbuz, M. S., Marsden, C. A., Hogg, S. L., & Blackburn-Munro, R. E. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01422.x · Cited by 257 · see citing works
Social Stress in Hamsters: Defeat Activates Specific Neurocircuits within the Brain
Kollack‐Walker, S., Watson, S. J., & Akil, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-22-08842.1997 · Cited by 253 · see citing works
Adaptation in patterns of c‐fos expression in the brain associated with exposure to either single or repeated social stress in male rats
Martı́nez, M., Phillips, P. J., & Herbert, J. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00011.x · Cited by 253 · see citing works
Prediction of Psychological Outcomes One Year After a Motor Vehicle Accident
Mayou, R., Bryant, B., & Ehlers, A. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.8.1231 · Cited by 251 · see citing works
Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635
Bagdy, G., Gráf, M., Anheuer, Z. E., Modos, E. A., & Kántor, S. (2001) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145701002632 · Cited by 247 · see citing works
The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine
Burghardt, N. S., Sullivan, G. M., McEwen, B. S., Gorman, J. M., & LeDoux, J. E. (2004) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.02.029 · Cited by 246 · see citing works
The Impact of the Nonpeptide Corticotropin-Releasing Hormone Antagonist Antalarmin on Behavioral and Endocrine Responses to Stress**This research was supported by NIMH Grant MH-50479 and the Undergraduate Research Opportunities Program at the University of Colorado at Boulder.
Deak, T., Nguyen, K. T., Ehrlich, A. L., Watkins, L. R., Spencer, R. L., Maier, S. F., Licinio, J., Wong, M.-L., Chrousos, G. P., Webster, E., et al. (1999) · Endocrinology · doi:10.1210/endo.140.1.6415 · Cited by 242 · see citing works
Conditioned defeat in male and female syrian hamsters
Huhman, K. L., Solomon, M. B., Janicki, M., Harmon, A. C., Lin, S. M., Israel, J. E., & Jasnow, A. M. (2003) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.05.001 · Cited by 239 · see citing works
Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): Roles for PACAP in anxiety-like behavior
Hammack, S. E., Cheung, J., Rhodes, K. M., Schutz, K. C., Falls, W. A., Braas, K. M., & May, V. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.12.013 · Cited by 231 · see citing works
Self-citation
Role of the extended amygdala in short-duration versus sustained fear: a tribute to Dr. Lennart Heimer
Walker, D. L., & Davis, M. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0183-3 · Cited by 231 · see citing works
Effects of Corticotropin-Releasing Factor on Brain Serotonergic Activity
M Price, B. A. (1998) · Neuropsychopharmacology · doi:10.1016/s0893-133x(97)00197-8 · Cited by 226 · see citing works
Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat
Amat, J., Matus-Amat, P., Watkins, L. R., & Maier, S. F. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00960-3 · Cited by 222 · see citing works
Posttraumatic stress disorder, exposure to combat, and lower plasma cortisol among Vietnam veterans: Findings and clinical implications.
Boscarino, J. A. (1996) · Journal of Consulting and Clinical Psychology · doi:10.1037//0022-006x.64.1.191 · Cited by 222 · see citing works
Post-traumatic stress disorder and depression: An analysis of comorbidity
Bleich, A., Koslowsky, M., Dolev, A., & Lerer, B. (1997) · British Journal of Psychiatry · doi:10.1192/bjp.170.5.479 · Cited by 211 · see citing works
Corticotropin-Releasing Factor IncreasesIn VitroFiring Rates of Serotonergic Neurons in the Rat Dorsal Raphe Nucleus: Evidence for Activation of a Topographically Organized Mesolimbocortical Serotonergic System
Lowry, C. A., Rodda, J. E., Lightman, S. L., & Ingram, C. D. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07728.2000 · Cited by 211 · see citing works
A Neurochemically Distinct Dorsal Raphe-Limbic Circuit with a Potential Role in Affective Disorders
Commons, K. G., Connolley, K. R., & Valentino, R. J. (2002) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300045 · Cited by 211 · see citing works
Bidirectional connections of the medial amygdaloid nucleus in the Syrian hamster brain: Simultaneous anterograde and retrograde tract tracing
Coolen, L. M., & Wood, R. I. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980921)399:2 · Cited by 207 · see citing works
Amplified behavioral and endocrine responses to forced swim stress in the Wistar–Kyoto rat
Rittenhouse, P. A., López‐Rubalcava, C., Stanwood, G. D., & Lucki, I. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00052-x · Cited by 207 · see citing works
Effects of trauma exposure on the cortisol response to dexamethasone administration in PTSD and major depressive disorder
Yehuda, R., Halligan, S. L., Golier, J. A., Grossman, R., & Bierer, L. M. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00052-0 · Cited by 206 · see citing works
5-Hydroxytryptamine 2C Receptors in the Basolateral Amygdala Are Involved in the Expression of Anxiety After Uncontrollable Traumatic Stress
Christianson, J. P., Ragole, T., Amat, J., Greenwood, B. N., Strong, P. V., Paul, E. D., Fleshner, M., Watkins, L. R., & Maier, S. F. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.011 · Cited by 204 · see citing works
Differential expression of 5HT‐1A, α1b adrenergic, CRF‐R1, and CRF‐R2 receptor mRNA in serotonergic, γ‐aminobutyric acidergic, and catecholaminergic cells of the rat dorsal raphe nucleus
Day, H. E. W., Greenwood, B. N., Hammack, S. E., Watkins, L. R., Fleshner, M., Maier, S. F., & Campeau, S. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20138 · Cited by 201 · see citing works
Self-citation
Escape performance following exposure to inescapable shock: Deficits in motor response maintenance.
Anisman, H., deCatanzaro, D., & Remington, G. J. (1978) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.4.3.197 · Cited by 200 · see citing works
Anxiety enhancement in the murine elevated plus maze by immediate prior exposure to social stressors
Rodgers, R. J., & Cole, J. C. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90222-2 · Cited by 200 · see citing works
Social stress in tree shrews
Fuchs, E., & Flügge, G. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00795-5 · Cited by 188 · see citing works
Role of CRF 1 and CRF 2 receptors in fear and anxiety
Takahashi, L. K. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00046-x · Cited by 186 · see citing works
Posttraumatic Stress Disorder: Clinical Features, Pathophysiology, and Treatment
Vieweg, W. V. R., Julius, D. A., Fernandez, A., Beatty-Brooks, M., Hettema, J. M., & Pandurangi, A. K. (2006) · The American Journal of Medicine · doi:10.1016/j.amjmed.2005.09.027 · Cited by 186 · see citing works
Emotional Memory: In Search of Systems and Synapsesa
LeDoux, J. E. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb17246.x · Cited by 184 · see citing works
Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: Aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear.
Waddell, J., Morris, R. W., & Bouton, M. E. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.2.324 · Cited by 183 · see citing works
The Role of Corticotropin‐Releasing Factor in the Pathophysiology of Affective and Anxiety Disorders: Laboratory and Clinical Studies
Owens, M. J., & Nemeroff, C. B. (2007) · Novartis Foundation symposium · doi:10.1002/9780470514368.ch15 · Cited by 181 · see citing works
Lesions of structures showing FOS expression to cat presentation: Effects on responsivity to a Cat, Cat odor, and nonpredator threat
Blanchard, D. C., Canteras, N. S., Markham, C. M., Pentkowski, N. S., & Blanchard, R. J. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.019 · Cited by 179 · see citing works
The role of the amygdala and dorsal raphe nucleus in mediating the behavioral consequences of inescapable shock.
Maier, S. F., Grahn, R. E., Kalman, B. A., Sutton, L. C., Wiertelak, E. P., & Watkins, L. R. (1993) · Behavioral Neuroscience · doi:10.1037//0735-7044.107.2.377 · Cited by 177 · see citing works
Behavioral and physiological characterization of male mice under chronic psychosocial stress
Bartolomucci, A., Pederzani, T., Sacerdote, P., Panerai, A. E., Parmigiani, S., & Palanza, P. (2003) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2003.08.003 · Cited by 177 · see citing works
Corticotropin Releasing Hormone Type 2 Receptors in the Dorsal Raphe Nucleus Mediate the Behavioral Consequences of Uncontrollable Stress
Hammack, S. E., Schmid, M. J., LoPresti, M. L., Der‐Avakian, A., Pelleymounter, M. A., Foster, A. C., Watkins, L. R., & Maier, S. F. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-03-01019.2003 · Cited by 176 · see citing works
Self-citation
Reduction of Stress-Induced Behavior by Antagonism of Corticotropin-Releasing Hormone 2 (CRH2) Receptors in Lateral Septum or CRH1Receptors in Amygdala
Bakshi, V. P., Smith-Roe, S., Newman, S. M., Grigoriadis, D. E., & Kalin, N. H. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02926.2002 · Cited by 171 · see citing works
Early life stress paradigms in rodents: potential animal models of depression?
Schmidt, M. V., Wang, X., & Meijer, O. C. (2010) · Psychopharmacology · doi:10.1007/s00213-010-2096-0 · Cited by 171 · see citing works
Medial amygdala modulation of predator odor-induced unconditioned fear in the rat.
Li, C.-I., Maglinao, T. L., & Takahashi, L. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.324 · Cited by 171 · see citing works
Posttraumatic stress disorder, exposure to combat, and lower plasma cortisol among Vietnam veterans: Findings and clinical implications.
Boscarino, J. A. (1996) · Journal of Consulting and Clinical Psychology · doi:10.1037/0022-006x.64.1.191 · Cited by 170 · see citing works
Early life experience alters behavior during social defeat: Focus on serotonergic systems
Gardner, K. L., Thrivikraman, K. V., Lightman, S. L., Plotsky, P. M., & Lowry, C. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.042 · Cited by 169 · see citing works
8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock.
Maier, S. F., Grahn, R. E., & Watkins, L. R. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.3.404 · Cited by 167 · see citing works
The Role of Corticotropin-Releasing Hormone in the Dorsal Raphe Nucleus in Mediating the Behavioral Consequences of Uncontrollable Stress
Hammack, S. E., Richey, K. J., Schmid, M. J., LoPresti, M. L., Watkins, L. R., & Maier, S. F. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-01020.2002 · Cited by 167 · see citing works
Self-citation
Exercise, Learned Helplessness, and the Stress-Resistant Brain
Greenwood, B. N., & Fleshner, M. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8029-y · Cited by 159 · see citing works
Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat
Amat, J., Matus-Amat, P., Watkins, L. R., & Maier, S. F. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00368-0 · Cited by 158 · see citing works
Acute and repeated exposure to social conflict in male golden hamsters: Increases in plasma POMC-peptides and cortisol and decreases in plasma testosterone
Huhman, K. L., Moore, T. O., Ferris, C. F., Mougey, E. H., & Meyerhoff, J. L. (1991) · Hormones and Behavior · doi:10.1016/0018-506x(91)90051-i · Cited by 154 · see citing works
Pleiotropic Functions of PACAP in the CNS
Shioda, S., Ohtaki, H., Nakamachi, T., Dohi, K., Watanabe, J., Nakajo, S., Arata, S., Kitamura, S., Okuda, H., Takenoya, F., et al. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1317.080 · Cited by 151 · see citing works
Stressor controllability and the pituitary-adrenal system.
Maier, S. F., Ryan, S. M., Barksdale, C. M., & Kalin, N. H. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.5.669 · Cited by 150 · see citing works
Differential effects of social stress on central serotonergic activity and emotional reactivity in Lewis and spontaneously hypertensive rats
Berton, O., Aguerre, S., Sarrieau, A., Mormède, P., & Chaouloff, F. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00282-0 · Cited by 147 · see citing works
Decrease in Brain Serotonin 2 Receptor Binding in Patients With Major Depression Following Desipramine Treatment
Yatham, L. N., Liddle, P. F., Dennie, J., Shiah, I., Adam, M. J., Lane, C. J., Lam, R. W. M., & Ruth, T. J. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.8.705 · Cited by 147 · see citing works
Social Stress in Tree Shrews as an Animal Model of Depression: An Example of a Behavioral Model of a CNS Disorder
Fuchs, E. (2005) · CNS Spectrums · doi:10.1017/s1092852900010038 · Cited by 145 · see citing works
The consequences of uncontrollable stress are sensitive to duration of prior wheel running
Greenwood, B. N., Foley, T. E., Burhans, D., Maier, S. F., & Fleshner, M. (2005) · Brain Research · doi:10.1016/j.brainres.2004.11.037 · Cited by 141 · see citing works
8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock.
Maier, S. F., Grahn, R. E., & Watkins, L. R. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.3.404 · Cited by 136 · see citing works
Exposure to the stressor environment prevents the temporal dissipation of behavioral depression/learned helplessness
Maier, S. F. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01095-7 · Cited by 135 · see citing works
The role of the amygdala and dorsal raphe nucleus in mediating the behavioral consequences of inescapable shock.
Maier, S. F., Grahn, R. E., Kalman, B. A., et al. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.2.377 · Cited by 134 · see citing works
Chemical Lesion of the Bed Nucleus of the Stria Terminalis Blocks the Behavioral Consequences of Uncontrollable Stress.
Hammack, S. E., Richey, K. J., Watkins, L. R., & Maier, S. F. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.443 · Cited by 130 · see citing works
Self-citation
Serotonin regulation of aggressive behavior in male golden hamsters (Mesocricetus auratus).
Ferris, C. F., Stolberg, T. L., & Delville, Y. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.4.804 · Cited by 130 · see citing works
Stressor controllability and the pituitary-adrenal system.
Maier, S. F., Ryan, S. M., Barksdale, C. M., et al. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.5.669 · Cited by 127 · see citing works
Corticotropin‐releasing factor in the dorsal raphe nucleus increases medial prefrontal cortical serotonin via type 2 receptors and median raphe nucleus activity
Forster, G. L., Pringle, R. B., Mouw, N. J., Vuong, S. M., Watt, M. J., Burke, A. R., Lowry, C. A., Summers, C. H., & Renner, K. J. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06333.x · Cited by 125 · see citing works
Roles for Pituitary Adenylate Cyclase-Activating Peptide (PACAP) Expression and Signaling in the Bed Nucleus of the Stria Terminalis (BNST) in Mediating the Behavioral Consequences of Chronic Stress
Hammack, S. E., Roman, C. W., Lezak, K. R., Kocho-Schellenberg, M., Grimmig, B. A., Falls, W. A., Braas, K. M., & May, V. (2010) · Journal of Molecular Neuroscience · doi:10.1007/s12031-010-9364-7 · Cited by 125 · see citing works
Self-citation
Microinjection of urocortin 2 into the dorsal raphe nucleus activates serotonergic neurons and increases extracellular serotonin in the basolateral amygdala
Amat, J., Tamblyn, J. P., Paul, E. D., Bland, S. T., Amat, P., Foster, A. C., Watkins, L. R., & Maier, S. F. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.07.052 · Cited by 119 · see citing works
Involvement of Central Amygdalar and Bed Nucleus of the Stria Terminalis Corticotropin-Releasing Factor in Behavioral Responses to Social Defeat.
Jasnow, A. M., Davis, M., & Huhman, K. L. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.5.1052 · Cited by 118 · see citing works
Stressor controllability, social interaction, and benzodiazepine systems
Short, K. R., & Maier, S. F. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90128-g · Cited by 117 · see citing works
Psychobiology of Stress
(1990) · Springer eBooks · doi:10.1007/978-94-009-1990-7 · Cited by 115 · see citing works
The Effects of Social Defeat and Other Stressors on the Expression of Circadian Rhythms
Meerlo, P., Sgoifo, A., & Turek, F. W. (2002) · Stress · doi:10.1080/102538902900012323 · Cited by 111 · see citing works
Prolonged and site-specific over-expression of corticotropin-releasing factor reveals differential roles for extended amygdala nuclei in emotional regulation
Regev, L., Neufeld-Cohen, A., Tsoory, M., Kuperman, Y., Getselter, D., Gil, S., & Chen, A. (2011) · Molecular Psychiatry · doi:10.1038/mp.2010.64 · Cited by 110 · see citing works
The role of prior stressor controllability and the dorsal raphé nucleus in sucrose preference and social exploration
Christianson, J. P., Paul, E. D., Irani, M., Thompson, B. M., Kubala, K. H., Yirmiya, R., Watkins, L. R., & Maier, S. F. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.04.024 · Cited by 107 · see citing works
Corticotropin-Releasing Factor Increases GABA Synaptic Activity and Induces Inward Current in 5-Hydroxytryptamine Dorsal Raphe Neurons
Kirby, L. G., Freeman-Daniels, E., Lemos, J. C., Nunan, J. D., Lamy, C. M., Akanwa, A. C., & Beck, S. G. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2887-08.2008 · Cited by 107 · see citing works
Recognition of Familiar Individuals in Golden Hamsters: A New Method and Functional Neuroanatomy
Lai, W., Ramiro, L.-L. R., Yu, H. A., & Johnston, R. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2124-05.2005 · Cited by 104 · see citing works
The response of neurons in the bed nucleus of the stria terminalis to serotonin: Implications for anxiety
Hammack, S. E., Guo, J.-D., Hazra, R., Dabrowska, J., Myers, K. M., & Rainnie, D. G. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.05.013 · Cited by 103 · cited 5× · see citing works
“The recent finding that PACAP may mediate behavioral changes associated with LH as well as those associated with repeated stress (Hammack et al., 2009a) suggests that this peptidergic system may represent a promising new target for the development of therapeutic drugs in the treatment of disorders…”
BackgroundInfluentialSelf-citation
5HT1A receptors and pharmacotherapy. Is serotonin receptor down-regulation linked to the mechanism of action of antidepressant drugs?
Stahl, S. M. (1994) · PubMed · Cited by 101 · see citing works
Activation of GABAA receptors in the amygdala blocks the acquisition and expression of conditioned defeat in Syrian hamsters
Jasnow, A. M., & Huhman, K. L. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03054-2 · Cited by 99 · see citing works
Adverse experience during early life and adulthood interact to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus
Gardner, K. L., Hale, M. W., Oldfield, S., Lightman, S. L., Plotsky, P. M., & Lowry, C. A. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.07.055 · Cited by 94 · see citing works
Increased corticotropin-releasing factor concentrations in the bed nucleus of the stria terminalis of anhedonic rats
Stout, S. C., Mortas, P., Owens, M. J., Nemeroff, C. B., & Moreau, J.-L. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00412-x · Cited by 94 · see citing works
Adverse early life experience and social stress during adulthood interact to increase serotonin transporter mRNA expression
Gardner, K. L., Hale, M. W., Lightman, S. L., Plotsky, P. M., & Lowry, C. A. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.065 · Cited by 84 · see citing works
Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala.
Jasnow, A. M., Shi, C., Israel, J. E., Davis, M., & Huhman, K. L. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.1125 · Cited by 84 · see citing works
Interactions between 5-hydroxytryptamine receptor subtypes: Is a disturbed receptor balance contributing to the symptomatology of depression in humans?
Berendsen, H. H. G. (1995) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(94)00075-e · Cited by 82 · see citing works
The olfactory bulbectomized rat as a model of depression
Jancsár, S. M., & Leonard, B. E. (1983) · Palgrave Macmillan UK eBooks · doi:10.1007/978-1-349-06689-6_25 · Cited by 82 · see citing works
Urocortin 2 increases c-Fos expression in topographically organized subpopulations of serotonergic neurons in the rat dorsal raphe nucleus
Staub, D. R., Spiga, F., & Lowry, C. A. (2005) · Brain Research · doi:10.1016/j.brainres.2005.02.080 · Cited by 77 · see citing works
Injections of urocortin 1 into the basolateral amygdala induce anxiety-like behavior and c-Fos expression in brainstem serotonergic neurons
Spiga, F., Lightman, S. L., Shekhar, A., & Lowry, C. A. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.12.051 · Cited by 75 · see citing works
Chlordiazepoxide microinjected into the region of the dorsal raphe nucleus eliminates the interference with escape responding produced by inescapable shock whether administered before inescapable shock or escape testing.
Maier, S. F., Kalman, B. A., & Grahn, R. E. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.1.121 · Cited by 74 · see citing works
The Effect of Stressor Controllability on Stress‐Induced Neuropeptide mRNA Expression within the Paraventricular Nucleus of the Hypothalamus
Helmreich, Watkins, Deak, Maier, Akil, & Watson (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00300.x · Cited by 73 · see citing works
The dorsal raphe nucleus is a site of action mediating the behavioral effects of benzodiazepine receptor inverse agonist DMCM.
Maier, S. F., Busch, C. R., Maswood, S., Grahn, R. E., & al, E. (1995) · Behavioral Neuroscience · doi:10.1037//0735-7044.109.4.759 · Cited by 73 · see citing works
Social defeat stress activates medial amygdala cells that express type 2 corticotropin-releasing factor receptor mRNA
Fekete, É. M., Zhao, Y., Li, C., Sabino, V., Vale, W. W., & Zorrilla, E. P. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.078 · Cited by 70 · see citing works
Is the medial amygdala part of the neural circuit modulating conditioned defeat in Syrian hamsters?Preprint
Markham, C. M., & Huhman, K. L. (2008) · Learning & Memory · doi:10.1101/lm.768208 · Cited by 69 · see citing works
Inescapable shock induces resistance to the effects of dexamethasone
O’Connor, K. A., Johnson, J. D., Hammack, S. E., Brooks, L. M., Spencer, R. L., Watkins, L. R., & Maier, S. F. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00035-5 · Cited by 69 · see citing works
Self-citation
Genetic predisposition and the development of posttraumatic stress disorder in an animal model
King, J. A., Abend, S., & Edwards, E. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01071-x · Cited by 65 · see citing works
Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamstersPreprint
Markham, C. M., Taylor, S. L., & Huhman, K. L. (2010) · Learning & Memory · doi:10.1101/lm.1633710 · Cited by 65 · see citing works
Aggressive encounters alter the activation of serotonergic neurons and the expression of 5-HT1A mRNA in the hamster dorsal raphe nucleus
Cooper, M. A., Grober, M. S., Nicholas, C. R., & Huhman, K. L. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.03.084 · Cited by 60 · see citing works
Self-citation
Low doses of corticotropin-releasing hormone injected into the dorsal raphe nucleus block the behavioral consequences of uncontrollable stress
Hammack, S. E., Pepin, J. L., DesMarteau, J. S., Watkins, L. R., & Maier, S. F. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00133-5 · Cited by 60 · see citing works
Self-citation
Chlordiazepoxide microinjected into the region of the dorsal raphe nucleus eliminates the interference with escape responding produced by inescapable shock whether administered before inescapable shock or escape testing.
Maier, S. F., Kalman, B. A., & Grahn, R. E. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.121 · Cited by 55 · see citing works
Exercise is associated with reduction in the anxiogenic effect of mCPP on acoustic startle.
Fox, J. H., Hammack, S. E., & Falls, W. A. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.4.943 · Cited by 53 · see citing works
Self-citation
The dorsal raphe nucleus is a site of action mediating the behavioral effects of the benzodiazepine receptor inverse agonist DMCM.
Maier, S. F., Busch, C. R., Maswood, S., Grahn, R. E., & Watkins, L. R. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.4.759 · Cited by 53 · see citing works
Activation of 5-HT1A autoreceptors in the dorsal raphe nucleus reduces the behavioral consequences of social defeat
Cooper, M. A., McIntyre, K. E., & Huhman, K. L. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.06.009 · Cited by 52 · see citing works
Self-citation
Serotonin-CRF interaction in the bed nucleus of the stria terminalis: A light microscopic double-label immunocytochemical analysis
Phelix, C. F., Liposits, Z., & Paull, W. K. (1992) · Brain Research Bulletin · doi:10.1016/0361-9230(92)90217-l · Cited by 48 · see citing works
Electroconvulsive shock decreases binding to 5-HT2 receptors in nonhuman primates: An in vivo positron emission tomography study with [18F]setoperone
Strome, E. M., Clark, C. M., Zis, A. P., & Doudet, D. J. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.025 · Cited by 47 · see citing works
Role of the bed nucleus of the stria terminalis in the acquisition and expression of conditioned defeat in Syrian hamsters
Markham, C. M., Norvelle, A., & Huhman, K. L. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.10.022 · Cited by 44 · see citing works
Corticotropin-releasing factor type II (CRF₂) receptors in the bed nucleus of the stria terminalis modulate conditioned defeat in Syrian hamsters (Mesocricetus auratus).
Cooper, M. A., & Huhman, K. L. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.1042 · Cited by 42 · see citing works
Self-citation
Corticotropin-releasing factor receptors in the dorsal raphe nucleus modulate social behavior in Syrian hamsters
Cooper, M. A., & Huhman, K. L. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0849-1 · Cited by 41 · see citing works
Self-citation
NR2B subunit of the NMDA receptor in the basolateral amygdala is necessary for the acquisition of conditioned defeat in Syrian hamsters
Day, D. E., Cooper, M. A., Markham, C. M., & Huhman, K. L. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.09.034 · Cited by 40 · see citing works
Self-citation
Short and Long Term Physiological and Neurochemical Adaptations to Social Conflict
Miczek, K. A., Thompson, M. L., & Tornatzky, W. (1990) · Springer eBooks · doi:10.1007/978-94-009-1990-7_2 · Cited by 38 · see citing works
Effects of Social Stress on Hormones, Brain, and Behavior
Blanchard, D. C., McKittrick, C. R., Blanchard, R. J., & Hardy, M. P. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50015-9 · Cited by 33 · see citing works
Increased prevalence of negative life events in subtypes of major depressive disorder
Kohn, Y., Zislin, J., Agid, O., Hanin, B., Troudart, T., Shapira, B., Bloch, M., Gur, E., Ritsner, M. S., & Lerer, B. (2001) · Comprehensive Psychiatry · doi:10.1053/comp.2001.19753 · Cited by 28 · see citing works
Blocking corticotropin-releasing factor-2 receptors, but not corticotropin-releasing factor-1 receptors or glucocorticoid feedback, disrupts the development of conditioned defeat
Cooper, M. A., & Huhman, K. L. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.003 · Cited by 27 · see citing works
Self-citation
Effects of BNST lesions in female rats on forced swimming and navigational learning
Pezük, P., Aydin, E., Aksoy‐Aksel, A., & Canbeyli, R. S. (2008) · Brain Research · doi:10.1016/j.brainres.2008.06.071 · Cited by 26 · see citing works
BNST lesions aggravate behavioral despair but do not impair navigational learning in rats
Pezük, P., Aytürk, D. G., Aksoy‐Aksel, A., & Canbeyli, R. S. (2006) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2006.02.008 · Cited by 25 · see citing works

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Overshadowed by the amygdala: The bed nucleus of the stria terminalis emerges as key to psychiatric disorders
Lebow, M. A., & Chen, A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.1 · Cited by 660 · see citing works
Prefrontal cortex circuits in depression and anxiety: contribution of discrete neuronal populations and target regions
Hare, B. D., & Duman, R. S. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0685-9 · Cited by 366 · see citing works
Breaking bonds in male prairie vole: Long-term effects on emotional and social behavior, physiology, and neurochemistry
Sun, P., Smith, A. S., Lei, K., Liu, Y., & Wang, Z. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.02.016 · Cited by 141 · see citing works
Decreased SGK1 Expression and Function Contributes to Behavioral Deficits Induced by Traumatic Stress
Licznerski, P., Duric, V., Banasr, M., Alavian, K. N., Ota, K. T., Kang, H. J., Jonas, E. A., Ursano, R., Krystal, J. H., Duman, R. S., et al. (2015) · PLOS Biology · doi:10.1371/journal.pbio.1002282 · Cited by 79 · see citing works
Stress-sensitive inference of task controllability
Ligneul, R., Mainen, Z. F., Ly, V., & Cools, R. (2022) · Nature Human Behaviour · doi:10.1038/s41562-022-01306-w · Cited by 60 · see citing works
Learned stressor resistance requires extracellular signal-regulated kinase in the prefrontal cortex
Christianson, J. P., Flyer-Adams, J. G., Drugan, R. C., Amat, J., Daut, R. A., Foilb, A. R., Watkins, L. R., & Maier, S. F. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00348 · Cited by 39 · see citing works
Subjective Uncontrollability over Aversive Events Reduces Working Memory Performance and Related Large-Scale Network Interactions
Wanke, N., & Schwabe, L. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhz298 · Cited by 28 · see citing works
Effects of fluoxetine on CRF and CRF1 expression in rats exposed to the learned helplessness paradigm
Fernández Macedo, G. V., Cladouchos, M. L., Sifonios, L., Cassanelli, P. M., & Wikinski, S. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2859-x · Cited by 27 · see citing works
The bed nucleus of the stria terminalis as a brain correlate of psychological inflexibility in fibromyalgia
Feliu-Soler, A., Martínez-Zalacaín, I., Pérez-Aranda, A., Borràs, X., Andrés-Rodríguez, L., Sanabria-Mazo, J. P., Fayed, N., Stephan-Otto, C., Núñez, C., Soriano-Mas, C., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020374 · Cited by 8 · see citing works
“The BNST has also been implicated in behavioral changes associated with depression; in particular, BNST activity has been related to anhedonic behavior after chronic mild stress, whereas lesions in this structure block the onset of learned helplessness in preclinical models [52].”
Background
Long-lasting marked inhibition of periaqueductal gray-evoked defensive behaviors in inescapably-shocked rats
Quintino‐dos‐Santos, J. W., Müller, C. J. T., C. Santos, A. M., Tufik, S., Rosa, C. A., & Schenberg, L. C. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12410 · Cited by 7 · see citing works

Crh receptor priming in the bed nucleus of the stria terminalis (BNST) induces tph2 gene expression in the dorsomedial dorsal raphe nucleus and chronic anxiety
Donner, N. C., Davies, S. M., Fitz, S. D., Kienzle, D. M., Shekhar, A., & Lowry, C. A. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109730 · Cited by 28 · see citing works
Constitutive 5-HT2C receptor knock-out facilitates fear extinction through altered activity of a dorsal raphe-bed nucleus of the stria terminalis pathwayPreprint
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Authors: Hammack, S. E., Cooper, M. A., & Lezak, K. R.
Affiliations: University of Vermont (US)
University of Tennessee at Knoxville (US)
Corresponding author: Hammack, Sayamwong E.
ORCID: Hammack, Sayamwong E.
Cooper, Matthew A.
Lezak, Kimberly R.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2012-02
Volume: 62
Issue: 2
Pages: 565-575
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2011.02.024
PMC: PMC3433056
OpenAlex: W2152055098
Cited by: 142
References: 153
Citations by year: 2026: 1 · 2025: 7 · 2024: 6 · 2023: 10 · 2022: 10 · 2021: 10 · 2020: 13 · 2019: 12 · 2018: 10 · 2017: 9 · 2016: 8 · 2015: 12 · 2014: 15 · 2013: 11 · 2012: 7
FWCI: 1.04
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R21MH085230)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: learned helplessness, major depressive disorder, post-traumatic stress disorder, serotonergic system, dorsal raphe nucleus, amygdala, basolateral amygdala, central amygdala, bed nucleus of the stria terminalis, social defeat, animal models of depression, antidepressant treatment
MeSH terms: Animals, Behavior, Animal, Brain, Conditioning, Psychological, Disease Models, Animal, Dominance-Subordination, Fear, Cricetinae, Helplessness, Learned, Stress Disorders, Post-Traumatic, Mood Disorders, Rats

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Overlapping neurobiology of learned helplessness and conditioned defeat: Implications for PTSD and mood disorders

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