A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response
Open accessAbstract
A network of interconnected limbic forebrain cell groups, including the medial prefrontal cortex (mPFC) and hippocampal formation (HF), is known to shape adaptive responses to emotionally stressful experiences, including output of the hypothalamo-pituitary-adrenal (HPA) axis. While disruption of limbic HPA-inhibitory systems is implicated in stress-related psychiatric and systemic illnesses, progress in the field has been hampered by a lack of a systems-level understanding of the organization that provides for this regulation. Using rats, we first localized cell groups afferent to the paraventricular hypothalamic nucleus (PVH) (the initiator of HPA responses to stress) whose engagement following acute (30 min) restraint was diminished by excitotoxin lesions of the ventral subiculum, a component of the HF. This identified a candidate relay for imparting HF influences in a circumscribed portion of the anterior bed nucleus of the stria terminalis (aBST), which we previously identified as a GABAergic relay subserving mPFC inhibition of the stress axis. Anatomical tracing experiments then indicated that extrinsic projections from HF and mPFC converge onto regions of aBST that contain neurons that are both stress sensitive and PVH projecting. Two final experiments provided evidence that (1) HPA-inhibitory influences of mPFC and HF are additive and (2) aBST plays a more prominent inhibitory role than ventral subiculum over stress-induced HPA endpoints. These findings support the view that stress-inhibitory influences of mPFC and HF are exerted principally via convergence onto a common relay, as opposed to a serial, parallel, or more complex multisynaptic network.
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The hippocampus inhibits the HPA axis through its fornix outputs to the hypothalamus.
“The hippocampus inhibits the HPA axis through its fornix outputs to the hypothalamus (59, 63, 64).”
From Childhood Trauma, the HPA Axis and Psychiatric Illnesses: A Targeted Literature Synthesis (2022) · cites this paper as [64]
The Discussion section ‘Neural pathways subserving HF HPA-inhibitory influences’ says that damage to the hippocampus or fimbria/fornix exaggerates stress-induced HPA responses, supporting an inhibitory role. It does not establish that inhibition travels through fornix outputs to the hypothalamus; the paper instead identifies a ventral-subiculum-to-anterior-BST relay that projects to the paraventricular hypothalamic nucleus. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe amygdala is principally excitatory to HPA axis functioning, while the hippocampus is mostly inhibitory.
“While the amygdala is principally excitatory to HPA axis functioning, the hippocampus is mostly inhibitory (63–65).”
From Childhood Trauma, the HPA Axis and Psychiatric Illnesses: A Targeted Literature Synthesis (2022) · cites this paper as [64]
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Cites
Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures?
Fanselow, M. S., & Dong, H.-W. (2010) · Neuron · doi:10.1016/j.neuron.2009.11.031 · Cited by 3,358 · see citing works
de Nó, R. L. (1934) · Cited by 1,974 · see citing works
Hippocampal atrophy in recurrent major depression
Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., & Vannier, M. W. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.9.3908 · Cited by 1,932 · see citing works
Brain Maps: Structure of the Rat Brain
Swanson, L. W. (1992) · Medical Entomology and Zoology · Cited by 1,851 · see citing works
Willner, P. (1997) · Psychopharmacology · doi:10.1007/s002130050456 · Cited by 1,832 · see citing works
JACOBSON, L., & SAPOLSKY, R. (1991) · Endocrine Reviews · doi:10.1210/edrv-12-2-118 · Cited by 1,739 · see citing works
Brain maps: structure of the rat brain
Guillery, R. W. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90187-q · Cited by 1,677 · see citing works
(1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.7.973 · Cited by 1,610 · 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
Swanson, L. W., & Cowan, W. M. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901720104 · Cited by 1,571 · see citing works
Sesack, S. R., Deutch, A. Y., Roth, R. H., & Bunney, B. S. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902900205 · Cited by 1,568 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
Swanson, L. W., & Kuypers, H. G. J. M. (1980) · Journal of Comparative Neurology · doi:10.1002/cne.901940306 · Cited by 1,413 · see citing works
Why stress is bad for your brain
Sapolsky, R. M. (1996) · Science · doi:10.1126/science.273.5276.749 · Cited by 1,306 · cited 2× · see citing works
“…HPA-inhibitory influences contributes to the etiology of depression and other stress-related psychopathologies (Carroll et al., 1976; Bremner et al., 1995; Sapolsky, 1996; Sheline et al., 1996), progress has been hampered by the fact that the underlying neural substrates are poorly understood.”
BackgroundThe glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system
Shu, S., Ju, G., & Fan, L. (1988) · Neuroscience Letters · doi:10.1016/0304-3940(88)90346-1 · Cited by 1,235 · see citing works
Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons
Watanabe, Y., Gould, E., & McEwen, B. S. (1992) · Brain Research · doi:10.1016/0006-8993(92)91597-8 · Cited by 1,212 · see citing works
Diorio, D., Viau, V, & Meaney, M. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-09-03839.1993 · Cited by 1,151 · see citing works
Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging
Sapolsky, R., Krey, L., & McEwen, B. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01222.1985 · Cited by 1,129 · see citing works
Pattern and time course of immediate early gene expression in rat brain following acute stress
Cullinan, W. E., Herman, J. P., Battaglia, D. F., Akil, H., & Watson, S. J. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00355-9 · Cited by 1,056 · see citing works
Reduced fear expression after lesions of the ventral hippocampus
Kjelstrup, K. G., Tuvnes, F. A., Steffenach, H.-A., Murison, R., Moser, E. I., & Moser, M.-B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152112399 · Cited by 912 · see citing works
Antoni, F. A. (1986) · Endocrine Reviews · doi:10.1210/edrv-7-4-351 · Cited by 888 · see citing works
Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties
Schmued, L. C., & Fallon, J. H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91199-6 · Cited by 887 · see citing works
Plasticity of the Hippocampus: Adaptation to Chronic Stress and Allostatic Load
McEwen, B. S. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05830.x · Cited by 875 · see citing works
Simmons, D. M., Arriza, J. L., & Swanson, L. W. (1989) · Journal of Histotechnology · doi:10.1179/his.1989.12.3.169 · Cited by 872 · see citing works
Efferent projections of the infralimbic cortex of the rat
Hurley, K. M., Herbert, H., Moga, M. M., & Saper, C. B. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903080210 · Cited by 777 · see citing works
Sapolsky, R. M., Krey, L. C., & McEwen, B. S. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.19.6174 · Cited by 758 · see citing works
Selective Retention of Corticosterone by Limbic Structures in Rat Brain
McEwen, B. S., Weiss, J. M., & Schwartz, L. S. (1968) · Nature · doi:10.1038/220911a0 · Cited by 713 · see citing works
Neuroendocrine Regulation in Depression
Carroll, B. J. (1976) · Archives of General Psychiatry · doi:10.1001/archpsyc.1976.01770090029002 · Cited by 622 · see citing works
Canteras, N. S., & Swanson, L. W. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903240204 · Cited by 541 · see citing works
Cullinan, W. E., Herman, J. P., & Watson, S. J. (1993) · Journal of Comparative Neurology · doi:10.1002/cne.903320102 · Cited by 541 · see citing works
Dong, H., Petrovich, G. D., Watts, A. G., & Swanson, L. W. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1079 · Cited by 521 · see citing works
Dayas, C. V., Buller, K. M., Crane, J. W., Xu, Y., & Day, T. A. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01733.x · Cited by 514 · see citing works
Bhatnagar, S., & Dallman, M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00577-0 · Cited by 511 · see citing works
Herman, J. P., Schafer, M., Young, E. A., Thompson, R. C., DOUGLASS, J. O., Akil, H., & Watson, S. J. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-09-03072.1989 · Cited by 467 · see citing works
Radley, J. J., Arias, C. M., & Sawchenko, P. E. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4297-06.2006 · Cited by 456 · see citing works
Self-citationRIVIER, C. L., & Vale, W. (1983) · Endocrinology · doi:10.1210/endo-113-3-939 · Cited by 409 · 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
Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1
Dong, H., Swanson, L. W., Chen, L., Fanselow, M. S., & Toga, A. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812608106 · Cited by 361 · see citing works
Swanson, L. W., & Köhler, C. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-10-03010.1986 · Cited by 340 · see citing works
Roland, B. L., & Sawchenko, P. E. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903320109 · Cited by 334 · see citing works
Self-citationPhysiological Mapping of Local Inhibitory Inputs to the Hypothalamic Paraventricular Nucleus
Boudaba, C., Szabó, K., & Tasker, J. G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-22-07151.1996 · Cited by 333 · see citing works
Kovacs, K., & Sawchenko, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-01-00262.1996 · Cited by 310 · see citing works
Self-citationDong, H.-W., & Swanson, L. W. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20788 · Cited by 290 · see citing works
RIVIER, C. L., Rivier, J., & Vale, W. (1982) · Science · doi:10.1126/science.6289439 · Cited by 273 · see citing works
Paraventricular hypothalamic nucleus: Axonal projections to the brainstem
Geerling, J. C., Shin, J., Chimenti, P. C., & Loewy, A. D. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22283 · Cited by 273 · 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
Self-citationPathways to the Secretion of Adrenocorticotropin: A View from the Portal*
Plotsky, P. M. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00231.x · Cited by 258 · see citing works
Chronology for Fluctuations in Late Pleistocene Sierra Nevada Glaciers and Lakes
Phillips, F. M., Zreda, M., Benson, L. V., Plummer, M. A., Elmore, D., & Sharma, P. (1996) · Science · doi:10.1126/science.274.5288.749 · Cited by 245 · see citing works
Role of the ventral subiculum in stress integration
Herman, J. P., & Mueller, N. K. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.05.035 · Cited by 235 · see citing works
Campeau, S., Falls, W. A., Cullinan, W. E., Helmreich, D. L., Davis, M. E., & Watson, S. J. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00632-x · Cited by 230 · see citing works
Herman, J. P., Cullinan, W. E., Morano, M. I., Akil, H., & Watson, S. J. (1995) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1995.tb00784.x · Cited by 214 · see citing works
Feldman, S., & Conforti, N. (2008) · Neuroendocrinology · doi:10.1159/000122974 · Cited by 193 · see citing works
Herman, J. P., Dolgas, C. M., & Carlson, S. L. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00055-4 · Cited by 193 · see citing works
Walaas, I., & Fonnum, F. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90088-3 · Cited by 190 · see citing works
́cs, K. J. K., & Makara, G. B. (1988) · Brain Research · doi:10.1016/0006-8993(88)90435-0 · Cited by 185 · see citing works
Kovács, K. J., Földes, A., & Sawchenko, P. E. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03843.2000 · Cited by 172 · cited 2× · see citing works
“, 10 m) in the medial parvicellular subdivision that were overlain by reduced silver grains (more than three grains per nuclei) (Kovács et al., 2000).”
BackgroundMethodSelf-citationSpencer, S. J., Buller, K. M., & Day, T. A. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20376 · Cited by 171 · see citing works
Viau, V., & Sawchenko, P. E. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10178 · Cited by 153 · see citing works
Self-citationChronic stress plasticity in the hypothalamic paraventricular nucleus
Herman, J. P., Flak, J. N., & Jankord, R. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00429-9 · Cited by 149 · see citing works
Ottenweller, J. E., Natelson, B. H., Pitman, D. L., & Drastal, S. D. (1989) · Biological Psychiatry · doi:10.1016/0006-3223(89)90123-6 · Cited by 149 · see citing works
Radley, J. J., Williams, B., & Sawchenko, P. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0552-08.2008 · Cited by 148 · see citing works
Self-citationMa, X.-M., Levy, A., & Lightman, S. L. (1997) · Journal of Endocrinology · doi:10.1677/joe.0.1520081 · Cited by 136 · see citing works
Vitalis, T., Cases, O., Callebert, J., Launay, J., Price, D. J., Seif, I., & Gaspar, P. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980406)393:2 · Cited by 129 · see citing works
Two types of corticopulvinar terminations: Round (type 2) and elongate (type 1)
Rockland, K. S. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960422)368:1 · Cited by 129 · see citing works
Herman, J. P. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903630103 · Cited by 129 · see citing works
Jaferi, A., & Bhatnagar, S. (2006) · Endocrinology · doi:10.1210/en.2005-1393 · Cited by 122 · see citing works
Inputs to the ventrolateral bed nucleus of the stria terminalis
Shin, J., Geerling, J. C., & Loewy, A. D. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21870 · Cited by 115 · see citing works
Chang, H. T., Kuo, H.-K., Whittaker, J. A., & Cooper, N. G. F. (1990) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(90)90091-s · Cited by 90 · see citing works
Phaseolus vulgaris Leucoagglutinin Anterograde Axonal Transport Technique
Sawchenko, P. E., Cunningham, E. T., Mortrud, M. T., et al. (1990) · Methods in neurosciences · doi:10.1016/b978-0-12-185255-9.50018-3 · Cited by 49 · see citing works
Self-citationChanges of plasma and adrenal catecholamines and corticosterone in stressed rats with septal lesions
Dobrakovová, M., Květňanský, R., Torda, T., & Murgas, K. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90363-8 · Cited by 35 · see citing works
Priou, A., Oliver, C., & Grino, M. (1993) · European Journal of Endocrinology · doi:10.1530/acta.0.1280466 · Cited by 33 · see citing works
Mason, P., Back, S., & Fields, H. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-04023.1992 · Cited by 25 · see citing works
Feldman, S., Saphier, D., & Conforti, N. (1987) · Experimental Neurology · doi:10.1016/0014-4886(87)90075-6 · Cited by 18 · see citing works
Hohensee, S., Bleiß, W., & Duch, C. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.09.018 · Cited by 18 · see citing works
Feldman, S., & Conforti, N. (1981) · Experimental Brain Research · doi:10.1007/bf00237345 · Cited by 8 · see citing works
Day, H. E. W., Curran, E. J., Watson, S. J., & Akil, H. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19991011)413:1
Flagged first, then by citations
Cited by
Sorted by citations
Regulation of the Hypothalamic‐Pituitary‐Adrenocortical Stress Response
Herman, J. P., McKlveen, J. M., Ghosal, S., Kopp, B., Wulsin, A., Makinson, R., Scheimann, J., & Myers, B. (2016) · Comprehensive Physiology · doi:10.1002/cphy.c150015 · Cited by 1,819 · see citing works
Learned helplessness at fifty: Insights from neuroscience.
Maier, S. F., & Seligman, M. E. P. (2016) · Psychological Review · doi:10.1037/rev0000033 · Cited by 919 · see citing works
“There is a pathway from the ventromedial prefrontal cortex to the paraventricular nucleus, but it goes through a relay in the bed nucleus of the stria terminalis, rather than directly (Radley & Sawchenko, 2011).”
BackgroundLebow, M. A., & Chen, A. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.1 · Cited by 660 · see citing works
Teicher, M. H., Anderson, C. M., & Polcari, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115396109 · Cited by 639 · see citing works
Treadway, M. T., Waskom, M. L., Dillon, D. G., Holmes, A. J., Park, M. T. M., Chakravarty, M. M., Dutra, S. J., Polli, F. E., Iosifescu, D. V., Fava, M., et al. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.06.018 · Cited by 331 · see citing works
Myers, B., McKlveen, J. M., & Herman, J. P. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2013.12.003 · Cited by 318 · see citing works
Neural regulation of the stress response: glucocorticoid feedback mechanisms
Herman, J. P., McKlveen, J. M., Solomon, M. B., Carvalho-Netto, E., & Myers, B. (2012) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2012007500041 · Cited by 307 · 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
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
Kudo, T., Uchigashima, M., Miyazaki, T., Konno, K., Yamasaki, M., Yanagawa, Y., Minami, M., & Watanabe, M. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4057-12.2012 · Cited by 177 · see citing works
Childhood Trauma, the HPA Axis and Psychiatric Illnesses: A Targeted Literature Synthesis
Murphy, F., Nasa, A., Cullinane, D., Raajakesary, K., Gazzaz, A., Sooknarine, V., Haines, M., Roman, E., Kelly, L., O'Neill, A., et al. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.748372 · Cited by 181 · see citing works
“The hippocampus inhibits the HPA axis through its fornix outputs to the hypothalamus (59, 63, 64).”
BackgroundHigh-fat diet-induced metabolic disorders impairs 5-HT function and anxiety-like behavior in mice
Zemdegs, J., Quesseveur, G., Jarriault, D., Pénicaud, L., Fioramonti, X., & Guiard, B. P. (2016) · British Journal of Pharmacology · doi:10.1111/bph.13343 · Cited by 180 · see citing works
Neural Regulation of the Stress Response: The Many Faces of Feedback
Myers, B., McKlveen, J. M., & Herman, J. P. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9801-y · Cited by 175 · see citing works
“Hence, inhibition is thought to be mediated by activation of PVN-projecting GABAergic neurons in the BST, POA, DMH, and peri-PVN region (Cullinan et al. 1993; Choi et al. 2007; Radley and Sawchenko 2011).”
The physiological control of eating: signals, neurons, and networks
Watts, A. G., Kanoski, S. E., Sanchez-Watts, G., & Langhans, W. (2022) · Physiological Reviews · doi:10.1152/physrev.00028.2020 · Cited by 168 · see citing works
Silberman, Y., Matthews, R. T., & Winder, D. G. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2949-12.2013 · Cited by 144 · see citing works
GABAA receptor-acting neurosteroids: a role in the development and regulation of the stress response
Gunn, B. G., Cunningham, L., Mitchell, S. G., Swinny, J. D., Lambert, J. J., & Belelli, D. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.06.001 · Cited by 149 · see citing works
Hypothalamic-pituitary – adrenal axis-feedback control
Keller‐Wood, M. (2015) · Comprehensive Physiology · doi:10.1002/cphy.c140065 · Cited by 131 · see citing works
Developmental origins of cardiovascular disease: Impact of early life stress in humans and rodents
Murphy, M. O., Cohn, D. M., & Loria, A. S. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.018 · Cited by 117 · see citing works
The neurobiology of offensive aggression: Revealing a modular view
de Boer, S. F., Olivier, B., Veening, J., & Koolhaas, J. M. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.040 · Cited by 70 · see citing works
The role of biogenic amine signaling in the bed nucleus of the stria terminals in alcohol abuse
Kash, T. L. (2012) · Alcohol · doi:10.1016/j.alcohol.2011.12.004 · Cited by 58 · see citing works
“Recent studies from the Sawchenko group have confirmed this important interaction, demonstrating that the anterolateral BNST can integrate information from the medial prefrontal cortex and hippocampal formation and inhibit HPA axis output (Radley and Sawchenko, 2011).”
Hippocampus-dependent place learning enables spatial flexibility in C57BL6/N mice
Kleinknecht, K. R., Bedenk, B. T., Kaltwasser, S. F., Grünecker, B., Yen, Y.-C., Czisch, M., & Wotjak, C. T. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00087 · Cited by 46 · see citing works
Morrison, K. E., Bader, L. R., Clinard, C. T., Gerhard, D. M., Gross, S. E., & Cooper, M. A. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.05.041 · Cited by 41 · see citing works
Huang, Y., Shen, Z., Hu, L., Xia, F., Li, Y., Zhuang, J., Chen, P., & Huang, Q. (2016) · Psychiatry Research · doi:10.1016/j.psychres.2016.10.005 · Cited by 22 · see citing works
Munk, A., Reme, S. E., & Jacobsen, H. B. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.630422 · Cited by 16 · see citing works
- Authors
- Radley, J. J., & Sawchenko, P. E.
- Affiliations
- University of Iowa (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-06-29
- Volume
- 31
- Issue
- 26
- Pages
- 9683-9695
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3197245
- OpenAlex
- W2072261329
- Cited by
- 251
- References
- 77
- Citations by year
- 2026: 7 · 2025: 8 · 2024: 12 · 2023: 18 · 2022: 19 · 2021: 20 · 2020: 8 · 2019: 12 · 2018: 18 · 2017: 19 · 2016: 22 · 2015: 12 · 2014: 27 · 2013: 22 · 2012: 23
- FWCI
- 9.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health (DK-26741)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 26741, P01DK026741)
- 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 › Neuropeptides and Animal Physiology
- Keywords
- neuroendocrine stress response, hypothalamic-pituitary-adrenal axis, medial prefrontal cortex, hippocampal formation, ventral subiculum, paraventricular nucleus, restraint stress, excitotoxic lesions, limbic forebrain
- MeSH terms
- Animals, gamma-Aminobutyric Acid, Hippocampus, Hypothalamo-Hypophyseal System, Immunohistochemistry, Male, Neurons, Paraventricular Hypothalamic Nucleus, Pituitary-Adrenal System, Stress, Physiological, Rats, Sprague-Dawley, Prefrontal Cortex, In Situ Hybridization, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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