Stress-induced alterations in anxiety-like behavior and adaptations in plasticity in the bed nucleus of the stria terminalis
Open accessAbstract
In vulnerable individuals, exposure to stressors can result in chronic disorders such as generalized anxiety disorder (GAD), major depressive disorder (MDD), and post-traumatic stress disorder (PTSD). The extended amygdala is critically implicated in mediating acute and chronic stress responsivity and anxiety-like behaviors. The bed nucleus of the stria terminalis (BNST), a subregion of the extended amygdala, serves as a relay of corticolimbic information to the paraventricular nucleus of the hypothalamus (PVN) to directly influence the stress response. To investigate the influence of the corticosteroid milieu and housing conditions on BNST function, adult C57Bl/6J were either acutely or chronically administered corticosterone (CORT, 25mg/kg in sesame oil) or vehicle (sesame oil) or were group housed or socially isolated for 1 day (acute) or 6-8 weeks (chronic). To ascertain whether these stressors could influence anxiety-like behavior, studies were performed using the novel open-field (NOF) and the elevated zero maze (EZM) tests. To investigate potential associated changes in plasticity, alterations in BNST function were assessed using ex vivo extracellular field potential recordings in the (dorsal-lateral) dlBNST and a high frequency stimulus protocol to induce long-term potentiation (LTP). Our results suggest that chronic CORT injections and chronic social isolation housing conditions lead to an increase in anxiety-like behavior on the EZM and NOF. Chronically stressed mice also displayed a parallel blunting of LTP in the dlBNST. Conversely, acute social isolation housing had no effect on anxiety-like behavior but still resulted in a blunting of LTP in the dlBNST. Collectively, our results suggest acute and chronic stressors can have a distinct profile on plasticity in the BNST that is not uniformly associated with an increase in anxiety-like behavior.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
24 hr of social isolation results in a blunting of long-term potentiation (LTP) in the BNST.
“Indeed, 24 hr of social isolation results in a blunting of long-term potentiation (LTP) in the BNST (Conrad et al., 2011).”
From Dorsal raphe dopamine neurons represent the experience of social isolation (2016) · cites this paper as Conrad et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Stress and the brain: from adaptation to disease
de Kloet, E. R., Joëls, M., & Holsboer, F. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1683 · Cited by 4,621 · see citing works
The use of a plus-maze to measure anxiety in the mouse
Lister, R. G. (1987) · Psychopharmacology · doi:10.1007/bf00177912 · Cited by 2,617 · see citing works
The clinical significance of loneliness: a literature review
Heinrich, L. M., & Gullone, E. (2006) · Clinical Psychology Review · doi:10.1016/j.cpr.2006.04.002 · Cited by 1,986 · see citing works
McEwen, B. S., & Sapolsky, R. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80028-x · Cited by 1,889 · see citing works
Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06810.2002 · Cited by 1,662 · see citing works
Herman, J. P., Figueiredo, H., Mueller, N. K., Ulrich-Lai, Y., Ostrander, M. M., Choi, D. C., & Cullinan, W. E. (2003) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2003.07.001 · Cited by 1,586 · see citing works
Phasic vs Sustained Fear in Rats and Humans: Role of the Extended Amygdala in Fear vs Anxiety
Davis, M., Walker, D. L., Miles, L., & Grillon, C. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.109 · Cited by 1,488 · cited 1× · see citing works
“Importantly, the BNST has been implicated in longer-duration and sustained increases in anxiety-like behavior [7].”
BackgroundGlucocorticoid receptors in major depression: relevance to pathophysiology and treatment
Pariante, C. M., & Miller, A. H. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01088-x · Cited by 1,147 · see citing works
Goshen, I., Kreisel, T., Ben-Menachem-Zidon, O., Licht, T., Weidenfeld, J., Ben-Hur, T., & Yirmiya, R. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002055 · Cited by 762 · see citing works
The use of behavioral test batteries: Effects of training history
McIlwain, K. L., Merriweather, M. Y., Yuva-Paylor, L. A., & Paylor, R. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00528-5 · Cited by 579 · see citing works
Limbic Regulation of Hypothalamo‐Pituitary‐Adrenocortical Function during Acute and Chronic Stress
Jankord, R., & Herman, J. P. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1410.012 · Cited by 578 · see citing works
Morimoto, M., Morita, N., Ozawa, H., Yokoyama, K., & Kawata, M. (1996) · Neuroscience Research · doi:10.1016/s0168-0102(96)01105-4 · Cited by 475 · see citing works
Gregus, A., Wintink, A. J., Davis, A. C., & Kalynchuk, L. E. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.013 · Cited by 435 · see citing works
Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy
Mitra, R., & Sapolsky, R. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0705615105 · Cited by 409 · see citing works
Control of neuronal excitability by corticosteroid hormones
Joëls, M., & de Kloet, E. R. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90345-9 · Cited by 400 · see citing works
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
Long‐term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences
Võikar, V., Polus, A., Vasar, E., & Rauvala, H. (2004) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2004.00106.x · Cited by 359 · see citing works
Erb, S. M., & Stewart, J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-j0006.1999 · Cited by 347 · see citing works
Wallace, D. L., Han, M.-H., Graham, D. L., Green, T. A., Vialou, V., Iñiguez, S. D., Cao, J.-L., Kirk, A., Chakravarty, S., Kumar, A., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2257 · Cited by 342 · see citing works
Effects of glucocorticoids on hippocampal long‐term potentiation
Pavlides, C., Watanabe, Y., & McEwen, B. S. (1993) · Hippocampus · doi:10.1002/hipo.450030210 · Cited by 323 · see citing works
The neuroendocrinology of depression and chronic stress
Checkley, S. (1996) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a011570 · Cited by 323 · see citing works
Effects of chronic stress on dendritic arborization in the central and extended amygdala
Vyas, A., Bernal, S., & Chattarji, S. (2003) · Brain Research · doi:10.1016/s0006-8993(02)04162-8 · Cited by 291 · see citing works
Radley, J. J., Gosselink, K. L., & Sawchenko, P. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5924-08.2009 · Cited by 268 · see citing works
Wilkinson, M. B., Xiao, G., Kumar, A., LaPlant, Q., Renthal, W., Sikder, D., Kodadek, T. J., & Nestler, E. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0932-09.2009 · Cited by 262 · see citing works
Modification of hippocampal neurogenesis and neuroplasticity by social environments
Lü, L., Bao, G., Chen, H., Xia, P., Fan, X., Zhang, J., Pei, G., & Ma, L. (2003) · Experimental Neurology · doi:10.1016/s0014-4886(03)00248-6 · Cited by 238 · see citing works
Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis
Dunn, J. D. (1987) · Brain Research · doi:10.1016/0006-8993(87)91111-5 · Cited by 184 · see citing works
Corticosteroid receptors and neuroplasticity
Sousa, N., Cerqueira, J., & Almeida, O. F. X. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.06.007 · Cited by 166 · see citing works
Wiegert, O., Joëls, M., & Krugers, H. (2006) · Learning & Memory · doi:10.1101/lm.87706 · Cited by 162 · see citing works
Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens
Barrot, M., Wallace, D. L., Bolaños, C. A., Graham, D. L., Perrotti, L. I., Neve, R. L., Chambliss, H., Yin, J. C. P., & Nestler, E. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500587102 · Cited by 162 · see citing works
Glucocorticoid Dysregulations and Their Clinical Correlates: From Receptors to Therapeutics
Marques, A. H., Silverman, M. N., & Sternberg, E. M. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04987.x · Cited by 158 · see citing works
Dissociation of the morphological correlates of stress‐induced anxiety and fear
Pêgo, J. M., Morgado, P. F., Pinto, L., Cerqueira, J., Almeida, O. F. X., & Sousa, N. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06112.x · Cited by 146 · see citing works
Sousa, N., Madeira, M. D., & Paula-Barbosa, M. M. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00218-2 · Cited by 141 · see citing works
Joëls, M., & Krugers, H. J. (2007) · Neural Plasticity · doi:10.1155/2007/93202 · Cited by 138 · see citing works
Casada, J. H., & Dafny, N. (1991) · Brain Research Bulletin · doi:10.1016/0361-9230(91)90069-v · Cited by 128 · see citing works
Kash, T. L., Nobis, W. P., Matthews, R. T., & Winder, D. G. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4715-08.2008 · Cited by 125 · see citing works
Conway-Campbell, B. L., McKenna, M. A., Wiles, C. C., Atkinson, H. C., de Kloet, E. R., & Lightman, S. L. (2007) · Endocrinology · doi:10.1210/en.2007-0585 · Cited by 125 · see citing works
Operant Sensation Seeking Engages Similar Neural Substrates to Operant Drug Seeking in C57 Mice
Olsen, C. M., & Winder, D. G. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.226 · Cited by 111 · see citing works
Social isolation alters neuroinflammatory response to stroke
Karelina, K., Norman, G. J., Zhang, N., Morris, J. S., Peng, H., & DeVries, A. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810737106 · Cited by 110 · see citing works
Chourbaji, S., Zacher, C., Sanchis‐Segura, C., Spanagel, R., & Gass, P. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.003 · Cited by 106 · see citing works
Effects of stress and corticosterone on activity and plasticity in the amygdala
Kavushansky, A., & Richter‐Levin, G. (2006) · Journal of Neuroscience Research · doi:10.1002/jnr.21058 · Cited by 106 · see citing works
Sousa, N., Almeida, O. F. X., Holsboer, F., Paula-Barbosa, M. M., & Madeira, M. D. (1998) · Stress · doi:10.3109/10253899809167288 · Cited by 105 · see citing works
Kitchener, P., Di Blasi, F., Borrelli, E., & Piazza, P. V. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03267.x · Cited by 105 · see citing works
Pavlides, C., & McEwen, B. S. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02188-5 · Cited by 101 · see citing works
Behavioural Validation of a Light/Dark Choice Procedure for Testing Anti-Anxiety Agents
Misslin, R., Belzung, C., & Vogel, E. (1989) · Behavioural Processes · doi:10.1016/s0376-6357(89)80010-5 · Cited by 99 · see citing works
Francesconi, W. G., Berton, F., Repunte‐Canonigo, V., Hagihara, K., Thurbon, D., Lekić, D., Specio, S. E., Greenwell, T. N., Chen, S. A., Rice, K. C., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5129-08.2009 · Cited by 90 · see citing works
Corticosterone shifts different forms of synaptic potentiation in opposite directions
Krugers, H. J., Alfarez, D. N., Karst, H., Parashkouhi, K., van Gemert, N., & Joëls, M. (2005) · Hippocampus · doi:10.1002/hipo.20092 · Cited by 88 · see citing works
Weitlauf, C., Egli, R. E., Grueter, B. A., & Winder, D. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1181-04.2004 · Cited by 77 · see citing works
Sarnyai, Z. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09011.x · Cited by 70 · see citing works
Zhou, J., Zhang, F., & Zhang, Y. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02934-6 · Cited by 64 · see citing works
Shepard, J. D., Schulkin, J. A., & MYERS, D. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.019 · Cited by 50 · see citing works
Costello, J., & Kendrick, K. D. (2000) · Journal of Advanced Nursing · doi:10.1046/j.1365-2648.2000.01625.x · Cited by 48 · see citing works
Ciocca, D., Maurel, D., & Bosler, O. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00287.2001 · Cited by 47 · see citing works
Post-weaning social isolation of rats leads to a diminution of LTP in the CA1 to subiculum pathway
Roberts, L., & Greene, J. R. T. (2003) · Brain Research · doi:10.1016/j.brainres.2003.08.022 · Cited by 41 · see citing works
Girotti, M., Weinberg, M., & Spencer, R. L. (2007) · Endocrinology · doi:10.1210/en.2006-1304 · Cited by 40 · see citing works
Ashby, D. M., Habib, D., Dringenberg, H. C., Reynolds, J. N., & Beninger, R. J. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.03.041 · Cited by 39 · see citing works
Gendreau, P. L. (1998) · Neuropsychopharmacology · doi:10.1016/s0893-133x(97)00131-0 · Cited by 38 · see citing works
Social Isolation Selectively Increases Anxiety in Mice without Affecting Depression-like Behavior
Kwak, C., Lee, S., & Kaang, B. (2009) · Korean Journal of Physiology and Pharmacology · doi:10.4196/kjpp.2009.13.5.357 · Cited by 34 · see citing works
Gendreau, P. L., Petitto, J. M., Gariépy, J., & Lewis, M. H. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.2.424 · Cited by 25 · see citing works
Gendreau, P. L., Petitto, J. M., Gariépy, J., & Lewis, M. H. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.2.424 · Cited by 23 · see citing works
Shepard, J. D., Chambers, C. O., Busch, C., Mount, A., & Schulkin, J. A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.04.029 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Joëls, M., Sarabdjitsingh, R. A., & Karst, H. (2012) · Pharmacological Reviews · doi:10.1124/pr.112.005892 · Cited by 425 · see citing works
Dorsal raphe dopamine neurons represent the experience of social isolation
Matthews, G. A., Nieh, E. H., Vander Weele, C. M., Halbert, S. A., Pradhan, R. V., Yosafat, A. S., Glober, G. F., Izadmehr, E. M., Thomas, R. E., Lacy, G. D., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.040 · Cited by 402 · see citing works
Stress, anxiety, and dendritic spines: What are the connections?
Leuner, B., & Shors, T. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.021 · Cited by 284 · see citing works
Neural mechanisms of social homeostasis
Matthews, G. A., & Tye, K. M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14016 · Cited by 273 · see citing works
Functional heterogeneity in the bed nucleus of the stria terminalis
Gungor, N. Z., & Pare, D. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0856-16.2016 · Cited by 214 · see citing works
Stress Modulation of Opposing Circuits in the Bed Nucleus of the Stria Terminalis
Daniel, S., & Rainnie, D. G. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.178 · Cited by 213 · see citing works
Role of the bed nucleus of the stria terminalis in aversive learning and memoryPreprint
Goode, T. D., & Maren, S. (2017) · Learning & Memory · doi:10.1101/lm.044206.116 · Cited by 138 · see citing works
Stress-induced alterations in large-scale functional networks of the rodent brain
Henckens, M. J. A. G., van der Marel, K., van der Toorn, A., Pillai, A. G., Fernández, G., Dijkhuizen, R. M., & Joëls, M. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.10.037 · Cited by 110 · see citing works
Vachon, P., Millecamps, M., Low, L. A., Thompsosn, S. J., Pailleux, F., Beaudry, F., Bushnell, C. M., & Stone, L. S. (2013) · Behavioral and Brain Functions · doi:10.1186/1744-9081-9-22 · Cited by 111 · see citing works
Wills, T. A., Klug, J. R., Silberman, Y., Baucum, A. J., Weitlauf, C., Colbran, R. J., Delpire, E., & Winder, D. G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113820109 · Cited by 98 · see citing works
Concordance and incongruence in preclinical anxiety models: Systematic review and meta-analyses
Mohammad, F., Ho, J., Woo, J. H., Lim, C. L., Poon, D., Lamba, B., & Claridge‐Chang, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.04.011 · Cited by 73 · see citing works
Shukla, P. K., Meena, A. S., Dalal, K. K., Canelas, C., Samak, G., Pierre, J. F., & Rao, R. (2021) · Scientific Reports · doi:10.1038/s41598-020-80637-y · Cited by 64 · see citing works
Salimando, G. J., Hyun, M., Boyt, K. M., & Winder, D. G. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0270-20.2020 · Cited by 63 · see citing works
A Key Role for Neurotensin in Chronic-Stress-Induced Anxiety-Like Behavior in Rats
Normandeau, C. P., Ventura‐Silva, A. P., Hawken, E. R., Angelis, S., Sjaarda, C. P., Liu, X., Pêgo, J. M., & Dumont, É. C. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.134 · Cited by 62 · see citing works
Janitzky, K., D’Hanis, W., Kröber, A., & Schwegler, H. (2014) · Brain Research · doi:10.1016/j.brainres.2014.12.030 · Cited by 57 · see citing works
Glangetas, C., Massi, L., Fois, G. R., Jalabert, M., Girard, D., Diana, M., Yonehara, K., Roska, B., Xu, C., Lüthi, A., et al. (2017) · Nature Communications · doi:10.1038/ncomms14456 · Cited by 56 · see citing works
Role of the Bed Nucleus of the Stria Terminalis in PTSD: Insights From Preclinical Models
Miles, O. W., & Maren, S. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00068 · Cited by 57 · see citing works
Stress shifts the response of the bed nucleus of the stria terminalis to an anxiogenic mode
Ventura‐Silva, A. P., Pêgo, J. M., Sousa, J. C., Marques, A. R., Rodrigues, A. J., Marques, F., Cerqueira, J., Almeida, O. F. X., & Sousa, N. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08262.x · Cited by 52 · see citing works
Preclinical voluntary drinking models for alcohol abstinence‐induced affective disturbances in mice
Holleran, K. M., & Winder, D. G. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12338 · Cited by 53 · see citing works
Dabrowska, J., Hazra, R., Guo, J., Li, C., DeWitt, S., Xu, J., Lombroso, P. J., & Rainnie, D. G. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.032 · Cited by 53 · see citing works
Glangetas, C., Girard, D., Groc, L., Marsicano, G., Chaouloff, F., & Georges, F. E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3175-13.2013 · Cited by 51 · see citing works
Deguchi, Y., Harada, M., Shinohara, R., Lazarus, M., Chérasse, Y., Urade, Y., Yamada, D., Sekiguchi, M., Watanabe, D., Furuyashiki, T., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.088 · Cited by 46 · see citing works
Amygdalar expression of proteins associated with neuroplasticity in major depression and suicide
Maheu, M., Davoli, M. A., Turecki, G., & Mechawar, N. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.11.013 · Cited by 49 · see citing works
Rodríguez-Sierra, O. E., Turesson, H., & Paré, D. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00408.2013 · Cited by 46 · see citing works
Hazra, R., Guo, J. D., Dabrowska, J., & Rainnie, D. G. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.08.014 · Cited by 42 · see citing works
Neurobiological Trajectories Involving Social Isolation in PTSD: A Systematic Review
Vlachos, I. I., Papageorgiou, C., & Margariti, M. M. (2020) · Brain Sciences · doi:10.3390/brainsci10030173 · Cited by 40 · see citing works
Zilkha, N., Sofer, Y., Kashash, Y., & Kimchi, T. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.03.005 · Cited by 37 · see citing works
Facilitation of Serotonin Signaling by SSRIs is Attenuated by Social Isolation
Dankoski, E. C., Agster, K. L., Fox, M. E., Moy, S. S., & Wightman, R. M. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.162 · Cited by 36 · see citing works
A prefrontal-bed nucleus of the stria terminalis circuit limits fear to uncertain threat
Glover, L. R., McFadden, K. M., Bjorni, M., Smith, S. R., Rovero, N. G., Oreizi-Esfahani, S., Yoshida, T., Postle, A. F., Nonaka, M., Halladay, L. R., et al. (2020) · eLife · doi:10.7554/elife.60812 · Cited by 32 · see citing works
Cippitelli, A., Ayanwuyi, L. O., Barbier, E., Domi, E., Lerma-Cabrera, J. M., Carvajal, F., Scuppa, G., Li, H., Ubaldi, M., Heilig, M. A., et al. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3743-7 · Cited by 32 · see citing works
Sampedro‐Piquero, P., Begega, A., Zancada-Menéndez, C., Cuesta, M., & Arias, J. L. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.06.003 · Cited by 31 · see citing works
Wang, H., Bai, Y., Chen, Y.-C., Zhang, R., Wang, H., Zhang, Y., Gan, J.-L., Peng, Z., & Tan, Q. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117189 · Cited by 26 · see citing works
Rosinger, Z. J., Guzman, R. M. D., Jacobskind, J. S., Saglimbeni, B., Malone, M., Fico, D., Justice, N. J., Forni, P. E., & Zuloaga, D. G. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.112847 · Cited by 24 · see citing works
Heredia, L., Torrente, M., Domingo, J. L., & Colomina, M. T. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.06.021 · Cited by 25 · see citing works
Maita, I., Bazer, A. S., Blackford, J. U., & Samuels, B. A. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00026-1 · Cited by 23 · see citing works
Harris, N. A., & Winder, D. G. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00169 · Cited by 22 · see citing works
Maita, I., Roepke, T. A., & Samuels, B. A. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.903782 · Cited by 21 · see citing works
Talani, G., Biggio, G., & Sanna, E. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00056 · Cited by 21 · see citing works
Ressler, R. L., Goode, T. D., Evemy, C. G., & Maren, S. (2020) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2020.107281 · Cited by 18 · see citing works
Talani, G., Licheri, V., Masala, N., Follesa, P., Mostallino, M. C., Biggio, G., & Sanna, E. (2013) · Neurochemical Research · doi:10.1007/s11064-013-1216-8 · Cited by 17 · see citing works
Dickson, P. E., & Mittleman, G. (2021) · Scientific Reports · doi:10.1038/s41598-021-83574-6 · Cited by 16 · see citing works
Glangetas, C., Guillaumin, A., Ladevèze, E., Braine, A., Gauthier, M., Bonamy, L., Doudnikoff, É., Dhellemmes, T., Landry, M., Bézard, E., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-51389-4 · Cited by 15 · see citing works
Kasten, C. R., Holmgren, E. B., Lerner, M. R., & Wills, T. A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01285-y · Cited by 15 · see citing works
Chronic methylphenidate exposure during adolescence reduces striatal synaptic responses to ethanol
Crowley, N. A., Cody, P. A., Davis, M. I., Lovinger, D. M., & Mateo, Y. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12426 · Cited by 15 · see citing works
Stress-induced neural activation is altered during early withdrawal from chronic methamphetamine
Jacobskind, J. S., Rosinger, Z. J., Brooks, M. L., & Zuloaga, D. G. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.03.034 · Cited by 14 · see citing works
Microglial sex differences in innate high anxiety and modulatory effects of minocycline
Ugursu, B., Sah, A., Sartori, S. B., Popp, O., Mertins, P., Dunay, I. R., Kettenmann, H., Singewald, N., & Wolf, S. A. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.03.035 · Cited by 13 · see citing works
Smithers, H. E., Terry, J. R., Brown, J. T., & Randall, A. D. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.100143 · Cited by 13 · see citing works
Donovan, M. L., Chun, E. K., Liu, Y., & Wang, Z. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.802569 · Cited by 9 · see citing works
Carpenter, J. M., Brown, K. A., Diaz, A. N., Dockman, R. L., Benbow, R. A., Harn, D. A., Norberg, T., Wagner, J. J., & Filipov, N. M. (2021) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2021.107012 · Cited by 10 · see citing works
Trachtenberg, E., Ruzal, K., Sandbank, E., Bigelman, E., Ricon‐Becker, I., Cole, S. W., Ben‐Eliyahu, S., & Bartal, I. B.-A. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.10.005 · Cited by 8 · see citing works
Barbosa, A. R. C., Nunes, D., Lima, D., Colombo, F. A., Nunes, J., Orlandi, A. A. D. S., Rocha, G. D. S., Pereira, D. S., Corona, L., & de Brito, T. R. P. (2022) · Rejuvenation Research · doi:10.1089/rej.2022.0037 · Cited by 6 · see citing works
Ma, Y., Sardar, H., Benabou, M. E., Yu, A. C., Morningstar, A. R., Fajardo, R. N., Kandil, I. F., Rogers, E. T., Vassalli, A., Kauer, J. A., et al. (2025) · Biological Psychiatry Global Open Science · doi:10.1016/j.bpsgos.2025.100617 · Cited by 5 · see citing works
Rainnie, D. G., Hazra, R., Dabrowska, J., Guo, J., Li, C. C., DeWitt, S., & Muly, E. C. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23435 · Cited by 5 · see citing works
Jiang, B., Xue, C., Xiao, X., Zhang, J., Xie, C., Li, Y., Zhong, D., Zheng, Z., Pan, D.-C., Li, J., et al. (2025) · General Hospital Psychiatry · doi:10.1016/j.genhosppsych.2025.08.015 · Cited by 4 · see citing works
5-HT4 Receptor Subtype, β-Arrestin Level, and Rapid-Onset Effects of Antidepressant Drugs
Mendez-David, I., David, D. J., Guilloux, J.-P., Hen, R., & Gardier, A. M. (2015) · Neuromethods · doi:10.1007/978-1-4939-2187-4_6 · Cited by 4 · see citing works
Doyle, M. A., Salimando, G. J., Altemus, M. E., Badt, J. K., Bedenbaugh, M. N., Vardy, A. S., Adank, D. N., Park, A. S., & Winder, D. G. (2024) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.15432 · Cited by 3 · see citing works
Rybka, K. A., Lafrican, J. J., Meunier, P., Reilly, D. M., Parra, K. E., Colón, L. M., Poulos, A. M., & Zuloaga, D. G. (2025) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2025.107554 · Cited by 3 · see citing works
Degroat, T. J., Paladino, S., Samuels, B. A., & Roepke, T. A. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70041 · Cited by 4 · see citing works
Modulation of social valence by insular cortex activity during acute social isolation in mice
Hiyoshi, K., Matsushita, D., & Watabe, A. M. (2025) · Molecular Brain · doi:10.1186/s13041-025-01236-4 · Cited by 2 · see citing works
Carpenter, J. M., Brown, K. A., Veltmaat, L., Ludwig, H. D., Clay, K. B., Norberg, T., Harn, D. A., Wagner, J. J., & Filipov, N. M. (2022) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2022.100553 · Cited by 2 · see citing works
Shang, Y., Yang, J., Wang, B., Hu, J., Liu, H., Zhang, Z., Wang, K., & Sun, T.-T. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.06.029 · Cited by 2 · see citing works
Heredia, L., Torrente, M., & Domingo, J. L. (2014) · Journal of Pharmacological and Toxicological Methods · doi:10.1016/j.vascn.2014.01.006 · Cited by 1 · see citing works
de Almeida, A. P., Baldo, M. V. C., & Motta, S. C. (2021) · Research Square · doi:10.21203/rs.3.rs-788121/v1 · Cited by 1 · see citing works
Encoding social preference by interhemispheric neurons in the InsulaPreprint
Glangetas, C., Ladevèze, E., Guillaumin, A., Gauthier, M., Doudnikoff, É., Bézard, E., Taupignon, A., Baufreton, J., & Georges, F. E. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.15.520538 · Cited by 1 · see citing works
Whitaker, L. R., Hendrickson, L. M., & Morikawa, H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405941-2.00012-2
The role of the bed nucleus of the stria terminalis in fear and anxiety
Güngör, N. Z. (2016) · doi:10.7282/t36112n1
Parikh, N., Hu, K., Allam, O., Ihnat, J. M., Rancu, A. L., Boroumand, S., Persing, J., & Alperovich, M. (2024) · Child's Nervous System · doi:10.1007/s00381-024-06381-0
Ludwig, H. D., Carpenter, J. M., & Filipov, N. M. (2024) · Journal of Applied Toxicology · doi:10.1002/jat.4739
The bed nucleus of the stria terminalis as a neuromodulatory target for refractory epilepsy
Murray, J., Hong, E., Mulloy, S., & Nobis, W. P. (2026) · Frontiers in Network Physiology · doi:10.3389/fnetp.2026.1800427
Hak, J., Luijendijk, M. C. M., Drost, L., Schipper, L., Adan, R. A. H., & Kooij, K. L. (2026) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2026.107216
- Authors
- Conrad, K. L., Louderback, K. M., Gessner, C. P., & Winder, D. G.
- Affiliations
- Vanderbilt University (US)
- Corresponding author
- Conrad, Kelly L.
- ORCID
- Winder, Danny G.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 2011-08
- Volume
- 104
- Issue
- 2
- Pages
- 248-256
- ISSN
- 0031-9384 (ISSN-L)
- PMC
- PMC3118978
- OpenAlex
- W2095622480
- Cited by
- 71
- References
- 60
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 6 · 2022: 5 · 2021: 7 · 2020: 5 · 2019: 3 · 2018: 2 · 2017: 3 · 2016: 6 · 2015: 2 · 2014: 7 · 2013: 9 · 2012: 7
- FWCI
- 3.00
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Vanderbilt University
- National Institutes of Health (AA019455)
- National Institute on Alcohol Abuse and Alcoholism (R01AA019455, AA019455)
- National Institute of Mental Health (MH065215-08, T32MH064913, MH064913, T32MH065215)
- National Institute on Drug Abuse (DA019112, R01DA019112)
- National Institute of Neurological Disorders and Stroke (T32NS007491, NS07491)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- bed nucleus of the stria terminalis, anxiety-like behavior, chronic stress, acute stress, corticosterone, social isolation, housing conditions, long-term potentiation, synaptic plasticity, extended amygdala, paraventricular nucleus, corticosteroids, generalized anxiety disorder, major depressive disorder, post-traumatic stress disorder
- MeSH terms
- Adaptation, Physiological, Analysis of Variance, Animals, Anxiety, Behavior, Animal, Biophysics, Corticosterone, Disease Models, Animal, Electric Stimulation, Exploratory Behavior, Male, Mice, Inbred C57BL, Septal Nuclei, Social Isolation, Time Factors, Long-Term Potentiation, Patch-Clamp Techniques, Maze Learning, Mice, In Vitro Techniques
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