The DOI matches its Crossref record; 93 of the 93 references it cites were found in a registry or an index.
Dysfunctional Astrocytic and Synaptic Regulation of Hypothalamic Glutamatergic Transmission in a Mouse Model of Early-Life Adversity: Relevance to Neurosteroids and Programming of the Stress Response
Open accessAbstract
Adverse early-life experiences, such as poor maternal care, program an abnormal stress response that may involve an altered balance between excitatory and inhibitory signals. Here, we explored how early-life stress (ELS) affects excitatory and inhibitory transmission in corticotrophin-releasing factor (CRF)-expressing dorsal-medial (mpd) neurons of the neonatal mouse hypothalamus. We report that ELS associates with enhanced excitatory glutamatergic transmission that is manifested as an increased frequency of synaptic events and increased extrasynaptic conductance, with the latter associated with dysfunctional astrocytic regulation of glutamate levels. The neurosteroid 5α-pregnan-3α-ol-20-one (5α3α-THPROG) is an endogenous, positive modulator of GABAA receptors (GABAARs) that is abundant during brain development and rises rapidly during acute stress, thereby enhancing inhibition to curtail stress-induced activation of the hypothalamic-pituitary-adrenocortical axis. In control mpd neurons, 5α3α-THPROG potently suppressed neuronal discharge, but this action was greatly compromised by prior ELS exposure. This neurosteroid insensitivity did not primarily result from perturbations of GABAergic inhibition, but rather arose functionally from the increased excitatory drive onto mpd neurons. Previous reports indicated that mice (dams) lacking the GABAAR δ subunit (δ(0/0)) exhibit altered maternal behavior. Intriguingly, δ(0/0) offspring showed some hallmarks of abnormal maternal care that were further exacerbated by ELS. Moreover, in common with ELS, mpd neurons of δ(0/0) pups exhibited increased synaptic and extrasynaptic glutamatergic transmission and consequently a blunted neurosteroid suppression of neuronal firing. This study reveals that increased synaptic and tonic glutamatergic transmission may be a common maladaptation to ELS, leading to enhanced excitation of CRF-releasing neurons, and identifies neurosteroids as putative early regulators of the stress neurocircuitry.
Overview
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
Verification
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?
The cited source says what the claim attributes to it.
In the citing paper
“Studies in rodents show an inhibitory effect of allopregnanolone on the function of the HPA axis (77–79).”
From Higher Circulating Cortisol in the Follicular vs. Luteal Phase of the Menstrual Cycle: A Meta-Analysis (2020) · cites this paper as [78]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302
Effects of stress throughout the lifespan on the brain, behaviour and cognition
Lupien, S. J., McEwen, B. S., Gunnar, M. R., & Heim, C. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2639 · Cited by 6,256
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
Insights into the regulation of protein abundance from proteomic and transcriptomic analyses
Vogel, C., & Marcotte, E. M. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3185 · Cited by 4,195
Neural regulation of endocrine and autonomic stress responses
Ulrich-Lai, Y. M., & Herman, J. P. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2647 · Cited by 3,318
NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease
Paoletti, P., Bellone, C., & Zhou, Q. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3504 · Cited by 2,523
The HPA axis in major depression: classical theories and new developments
Pariante, C. M., & Lightman, S. L. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.06.006 · Cited by 2,009
Wisden, W., Laurie, D. J., Monyer, H., & Seeburg, P. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-03-01040.1992 · Cited by 1,543
Joëls, M., & Baram, T. Z. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2632 · Cited by 1,521
The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3138 · Cited by 1,393
Fritschy, J., & Mohler, H. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590111 · Cited by 1,244
Neurosteroids: endogenous regulators of the GABAA receptor
Belelli, D., & Lambert, J. J. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1703 · Cited by 1,159
Self-citation[6] Correction for liquid junction potentials in patch clamp experiments
Neher, E. (1992) · Methods in Enzymology · doi:10.1016/0076-6879(92)07008-c · Cited by 1,132
Li, N., Liu, R.-J., Dwyer, J. M., Banasr, M., Lee, B., Son, H., Li, X.-Y., Aghajanian, G., & Duman, R. S. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.015 · Cited by 1,082
Towards a glutamate hypothesis of depression
Sanacora, G., Treccani, G., & Popoli, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.07.036 · Cited by 1,036
Early Life Programming and Neurodevelopmental Disorders
Bale, T. L., Baram, T. Z., Brown, A. S., Goldstein, J. M., Insel, T. R., McCarthy, M. M., Nemeroff, C. B., Reyes, T. M., Simerly, R. B., Susser, E. S., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.028 · Cited by 961
Purdy, R. H., Morrow, A. L., Moore, P. H., & Paul, S. M. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.10.4553 · Cited by 951
Control of Glutamate Clearance and Synaptic Efficacy by Glial Coverage of Neurons
Oliet, S. H. R., Piet, R., & Poulain, D. A. (2001) · Science · doi:10.1126/science.1059162 · Cited by 623
Neurobiological and psychiatric consequences of child abuse and neglect
Heim, C., Shugart, M., Craighead, W. E., & Nemeroff, C. B. (2010) · Developmental Psychobiology · doi:10.1002/dev.20494 · Cited by 613
Pharmacological characterization of a novel cell line expressing human α4β3δ GABAA receptors
Brown, N. A., Kerby, J., Bonnert, T. P., Whiting, P. J., & Wafford, K. A. (2002) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704795 · Cited by 603
GABA: A dominant neurotransmitter in the hypothalamus
Decavel, C., & van den Pol, A. N. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903020423 · Cited by 575
Preskorn, S., Baker, B., Kolluri, S., Menniti, F. S., Krams, M., & Landen, J. W. (2008) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e31818a6cea · Cited by 524
A Novel Mouse Model for Acute and Long-Lasting Consequences of Early Life Stress
Rice, C. J., Sandman, C. A., Lenjavi, M. R., & Baram, T. Z. (2008) · Endocrinology · doi:10.1210/en.2008-0633 · Cited by 521
Mihalek, R., Banerjee, P., Korpi, E. R., Quinlan, J. J., Firestone, L. L., Mi, Z.-P., Lagenaur, C. F., Tretter, V. E., Sieghart, W., Anagnostaras, S., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12905 · Cited by 520
Neural Mechanisms of Stress Resilience and Vulnerability
Franklin, T. B., Saab, B. J., & Mansuy, I. M. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.016 · Cited by 500
GABAAR Plasticity during Pregnancy: Relevance to Postpartum Depression
Maguire, J., & Mody, I. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.019 · Cited by 437
Metabolic Control of Vesicular Glutamate Transport and Release
Juge, N., Gray, J. A., Omote, H., Miyaji, T., Inoue, T., Hara, C., Uneyama, H., Edwards, R. H., Nicoll, R. A., & Moriyama, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.002 · Cited by 401
Kaffman, A., & Meaney, M. J. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01730.x · Cited by 391
The influence of subunit composition on the interaction of neurosteroids with GABAA receptors
Belelli, D., Casula, A. M., Ling, A., & Lambert, J. J. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00172-7 · Cited by 335
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
Patchev, V. K., Shoaib, M., Holsboer, F., & Almeida, O. F. X. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90330-1 · Cited by 305
Cell-attached voltage-clamp and current-clamp recording and stimulation techniques in brain slices
Perkins, K. L. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.02.010 · Cited by 305
Barbaccia, M. L., Roscetti, G., Trabucchi, M., Mostallino, M. C., Concas, A., Purdy, R. H., & Biggio, G. (2008) · Neuroendocrinology · doi:10.1159/000126953 · Cited by 303 · cited 2×
“Intriguingly, neurosteroid levels change dynamically in response to stress challenges (Purdy et al., 1991; Barbaccia et al., 1996; Biggio et al., 2007) and therefore may “fine-tune” GABAAR function of PVN neurons to influence HPA axis activity.”
BackgroundFragmentation and Unpredictability of Early-Life Experience in Mental Disorders
Baram, T. Z., Davis, E. P., Obenaus, A., Sandman, C. A., Small, S. L., Solodkin, A., & Stern, H. S. (2012) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2012.11091347 · Cited by 292
Patchev, V (1996) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00096-6 · Cited by 283 · cited 1×
“Inhibition of mpd firing by physiological concentrations of 5 3 -THPROG may be relevant to the documented anxiolytic and stress-protective actions of neurosteroids (Patchev et al., 1994, 1996; Biggio et al., 2007; Gunn et al., 2011).”
BackgroundDi, S., Malcher‐Lopes, R., Marcheselli, V. L., Bazan, N. G., & Tasker, J. G. (2005) · Endocrinology · doi:10.1210/en.2005-0610 · Cited by 282
Functional role of local GABAergic influences on the HPA axis
Cullinan, W. E., Ziegler, D. R., & Herman, J. P. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0192-2 · Cited by 255
Zarate, C. A., Mathews, D., Ibrahim, L., Chaves, J. F., Marquardt, C., Ukoh, I., Jolkovsky, L., Brutsche, N. E., Smith, M. A., & Luckenbaugh, D. A. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.10.019 · Cited by 255
Sarkar, J., Wakefield, S., MacKenzie, G., Moss, S. J., & Maguire, J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2560-11.2011 · Cited by 254
Extrasynaptic GABA A Receptors of Thalamocortical Neurons: A Molecular Target for Hypnotics
Belelli, D., Peden, D. R., Rosahl, T. W., Wafford, K. A., & Lambert, J. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2679-05.2005 · Cited by 252
Self-citationAltered chloride homeostasis removes synaptic inhibitory constraint of the stress axis
Hewitt, S. A., Cusulin, J. I. W., Kurz, E. U., & Bains, J. S. (2009) · Nature Neuroscience · doi:10.1038/nn.2274 · Cited by 237
Stórustovu, S. I., & Ebert, B. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.092403 · Cited by 230
Patterns of mRNA and protein expression for 12 GABAA receptor subunits in the mouse brain
Hörtnagl, H., Tasan, R. O., Wieselthaler, A., Kirchmair, E., Sieghart, W., & Sperk, G. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.01.008 · Cited by 229
Ibrahim, L., DiazGranados, N., Jolkovsky, L., Brutsche, N., Luckenbaugh, D. A., Herring, W. J., Potter, W. Z., & Zarate, C. A. (2012) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e31825d70d6 · Cited by 220
Biag, J., Huang, Y., Gou, L., Hintiryan, H., Askarinam, A., Hahn, J. D., Toga, A. W., & Dong, H. (2012) · Journal of Comparative Neurology · doi:10.1002/cne.22698 · Cited by 205
Neurosteroids, stress and depression: Potential therapeutic opportunities
Zorumski, C. F., Paul, S. M., Izumi, Y., Covey, D. F., & Mennerick, S. J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.10.005 · Cited by 204
Physiological Evidence for Local Excitatory Synaptic Circuits in the Rat Hypothalamus
Boudaba, C., Schrader, L. A., & Tasker, J. G. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3396 · Cited by 187
Miklós, I. H., & Kovács, K. J. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00147-1 · Cited by 182
Shimamoto, K., Sakai, R., Takaoka, K., Yumoto, N., Nakajima, T., Amara, S. G., & Shigeri, Y. (2004) · Molecular Pharmacology · doi:10.1124/mol.65.4.1008 · Cited by 180
Kőrösi, A., Shanabrough, M., McClelland, S., Liu, Z.-W., Borók, E., Gao, X., Horváth, T. L., & Baram, T. Z. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4214-09.2010 · Cited by 174
Priebe, K., Brake, W. G., Romeo, R. D., Sisti, H. M., Mueller, A., McEwen, B. S., & Francis, D. D. (2005) · Developmental Psychobiology · doi:10.1002/dev.20098 · Cited by 168
Role of the paraventricular nucleus microenvironment in stress integration
Herman, J. P., Cullinan, W. E., Ziegler, D. R., & Tasker, J. G. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02133.x · Cited by 168
Repeated Stress Impairs Endocannabinoid Signaling in the Paraventricular Nucleus of the Hypothalamus
Cusulin, J. I. W., Kuzmiski, J. B., & Bains, J. S. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1046-10.2010 · Cited by 153
Hsu, F., Zhang, G.-J., Raol, Y. S. H., Valentino, R. J., Coulter, D. A., & Brooks‐Kayal, A. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2131679100 · Cited by 144
Luther, J. A., Daftary, S. S., Boudaba, C., Gould, G., Halmos, K. C., & Tasker, J. G. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00867.x · Cited by 140
Chronic stress‐induced neurotransmitter plasticity in the PVN
Flak, J. N., Ostrander, M. M., Tasker, J. G., & Herman, J. P. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22142 · Cited by 140
Shen, Q., Lal, R., Luellen, B. A., Earnheart, J. C., Andrews, A. M., & Luscher, B. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.04.024 · Cited by 139
Surface trafficking of N-methyl-d-aspartate receptors: Physiological and pathological perspectives
Groc, L., Bard, L., & Choquet, D. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.05.029 · Cited by 135
Prescott, S. A., B, T. J. S. A., & Koninck, Y. D. (2006) · Molecular Pain · doi:10.1186/1744-8069-2-32 · Cited by 134
Dysfunctional astrocytic regulation of glutamate transmission in a rat model of depression
Gómez‐Galán, M., Bundel, D. D., Eeckhaut, A. V., Smolders, I. J., & Lindskog, M. (2012) · Molecular Psychiatry · doi:10.1038/mp.2012.10 · Cited by 123
Patchev, V. K., Montkowski, A., Rouskova, D., Korányi, L., Holsboer, F., & Almeida, O. F. X. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119261 · Cited by 121
Neurosteroids and GABAA Receptor Interactions: A Focus on Stress
Gunn, B. G., Brown, A. R., Lambert, J. J., & Belelli, D. (2011) · Frontiers in Neuroscience · doi:10.3389/fnins.2011.00131 · Cited by 115
Self-citationRuiz, A. J., Campanac, E., Scott, R. S., Rusakov, D. A., & Kullmann, D. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2512 · Cited by 112
Glial Regulation of Neuronal Function: From Synapse to Systems Physiology
Tasker, J. G., Oliet, S. H. R., Bains, J. S., Brown, C. H., & Stern, J. E. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02259.x · Cited by 110
Cooper, E. J., Johnston, G. A. R., & Edwards, F. A. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00437.x · Cited by 109
Verkuyl, J. M., Karst, H., & Joëls, M. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03846.x · Cited by 97
The pathways from mother's love to baby's future
Kőrösi, A. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.027.2009 · Cited by 95
Stress, ethanol, and neuroactive steroids
Biggio, G., Concas, A., Follesa, P., Sanna, E., & Serra, M. (2007) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2007.04.005 · Cited by 86
Vicini, S., Losi, G., & Homanics, G. E. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00126-0 · Cited by 82
Tokuda, K., Izumi, Y., & Zorumski, C. F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1660-11.2011 · Cited by 82
Melnick, I. V., Pronchuk, N., Cowley, M. A., Grove, K. L., & Colmers, W. F. (2007) · Neuron · doi:10.1016/j.neuron.2007.10.034 · Cited by 81
Ulrich‐Lai, Y. M., Jones, K. R., Ziegler, D. R., Cullinan, W. E., & Herman, J. P. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22571 · Cited by 79
Grobin, A. C., Heenan, E. J., Lieberman, J. A., & Morrow, A. L. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-05-01832.2003 · Cited by 76
Ranna, M., Sinkkonen, S. T., Möykkynen, T. P., Uusi‐Oukari, M., & Korpi, E. R. (2006) · BMC Pharmacology · doi:10.1186/1471-2210-6-1 · Cited by 75
Poisbeau, P., FELTZ, P., & Schlichter, R. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022034 · Cited by 75
Schüle, C., Baghai, T. C., Eser, D., & Rupprecht, R. (2009) · Expert Review of Neurotherapeutics · doi:10.1586/ern.09.52 · Cited by 74
Fleming, T. M., Scott, V., Naskar, K., Joe, N., Brown, C. H., & Stern, J. E. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.207340 · Cited by 73
Alon, T., Zhou, L., Pérez, C. A., Garfield, A. S., Friedman, J. M., & Heisler, L. K. (2009) · Endocrinology · doi:10.1210/en.2009-0881 · Cited by 70
Grobin, A. C., & Morrow, A. L. (2001) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00242-5 · Cited by 69
Haage, D., & Johansson, S. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.1.143 · Cited by 68
Potapenko, E. S., Biancardi, V. C., Zhou, Y., & Stern, J. E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3936-12.2013 · Cited by 59
Biancardi, V. C., Campos, R. R., & Stern, J. E. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22256 · Cited by 58
Rapid neuromodulation by cortisol in the rat paraventricular nucleus: an in vitro study
Zaki, A., & Barrett‐Jolley, R. (2002) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0704832 · Cited by 53
Miklós, I. H., & Kovács, K. J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.027 · Cited by 51
Swinny, J. D., O'Farrell, E. M., Bingham, B. C., Piel, D., Valentino, R. J., & Beck, S. G. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114570999037x · Cited by 47
Self-citationAssociation of the GABRD gene and childhood‐onset mood disorders
Feng, Y., Kapornai, K., Kiss, É., Tamás, Z., Mayer, L., Baji, I., Daróczi, G., Benák, I., Kothencné, V. O., Dombóvári, E., et al. (2010) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2010.00598.x · Cited by 43
de Vasconcellos-Bittencourt, A. P. S., Vendite, D. A., Nassif, M., Crema, L. M., Frozza, R., Thomazi, A. P., Nieto, F. B., Wofchuk, S., Salbego, C., da Rocha, E. R., et al. (2011) · Neurochemical Research · doi:10.1007/s11064-011-0404-7 · Cited by 36
Verkuyl, J. M., & Joëls, M. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00401.2002 · Cited by 35
Synchronized bursts of miniature inhibitory postsynaptic currents
Popescu, I., Morton, L. A., Franco, A. J., Di, S., Ueta, Y., & Tasker, J. G. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2009.181461 · Cited by 28
Allopregnanolone enhancement of GABAergic transmission in rat medial preoptic area neurons
Uchida, S., Noda, E., Kakazu, Y., Mizoguchi, Y., Akaike, N., & Nabekura, J. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00049.2002 · Cited by 27
Yang, J. H., Li, L. H., Lee, S., Jo, I. H., Lee, S. Y., & Ryu, P. D. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01531.x · Cited by 20
Progesterone-transforming enzyme activity in the hypothalamus of the male rat
Eechaute, W., Dhooge, W., Gao, C., Calders, P., Rubens, R., Weyne, J., & Kaufman, J. (1999) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(99)00106-5 · Cited by 19
Womack, M. D., Pyner, S., & Barrett‐Jolley, R. (2006) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0706911 · Cited by 18
Cited by
Sorted by citations
Turecki, G., & Meaney, M. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.11.022 · Cited by 796
Modulation of the Hypothalamic-Pituitary-Adrenal Axis by Early Life Stress Exposure
van Bodegom, M., Homberg, J. R., & Henckens, M. J. A. G. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00087 · Cited by 606
Toward understanding how early-life stress reprograms cognitive and emotional brain networks
Chen, Y., & Baram, T. Z. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.181 · Cited by 474
Sheng, J. A., Bales, N. J., Myers, S. A., Bautista, A. I., Roueinfar, M., Hale, T. M., & Handa, R. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.601939 · Cited by 418
Walker, C., Bath, K. G., Joëls, M., Kőrösi, A., Larauche, M. H., Lucassen, P. J., Morris, M. J., Raineki, C., Roth, T. L., Sullivan, R. M., et al. (2017) · Stress · doi:10.1080/10253890.2017.1343296 · Cited by 432
Metadata
- Authors
- Gunn, B. G., Cunningham, L., Cooper, M. A., Corteen, N. L., Seifi, M., Swinny, J. D., Lambert, J. J., & Belelli, D.
- Affiliations
- University of Dundee (GB)
- University of Portsmouth (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-12-11
- Volume
- 33
- Issue
- 50
- Pages
- 19534-19554
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3858624
- OpenAlex
- W1994143964
- Cited by
- 151
- References
- 93
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 17 · 2023: 8 · 2022: 11 · 2021: 15 · 2020: 15 · 2019: 17 · 2018: 12 · 2017: 12 · 2016: 4 · 2015: 12 · 2014: 15 · 2013: 1
- FWCI
- 5.24
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Discovery Research Portal (University of Dundee) (publishedVersion)
- Solent University Research Portal (Solent University) (submittedVersion, other-oa)
- Funders
- Wellbeing of Women (RG1265)
- Tenovus
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council (11426)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- childhood adversity, astrocytes, extrasynaptic glutamate, neurosteroids, GABAergic inhibition, maternal care, hypothalamic-pituitary-adrenal axis, excitation-inhibition balance, neonatal mice
- MeSH terms
- Action Potentials, Animals, Astrocytes, Corticotropin-Releasing Hormone, Disease Models, Animal, Hypothalamus, Synaptic Transmission, Neurons, Receptors, GABA-A, Stress, Psychological, Synapses, Neurotransmitter Agents, Mice
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
