Brain metabolic alterations in mice subjected to postnatal traumatic stress and in their offspring
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Adverse environmental and social conditions early in life have a strong impact on health. They are major risk factors for mental diseases in adulthood and, in some cases, their effects can be transmitted across generations. The consequences of detrimental stress conditions on brain metabolism across generations are not well known. Using high-field (14.1 T) magnetic resonance spectroscopy, we investigated the neurochemical profile of adult male mice exposed to traumatic stress in early postnatal life and of their offspring, and of undisturbed control mice. We found that, relative to controls, early life stress-exposed mice have metabolic alterations consistent with neuronal dysfunction, including reduced concentration of N-acetylaspartate, glutamate and γ-aminobutyrate, in the prefrontal cortex in basal conditions. Their offspring have normal neurochemical profiles in basal conditions. Remarkably, when challenged by an acute cold swim stress, the offspring has attenuated metabolic responses in the prefrontal cortex, hippocampus and striatum. In particular, the expected stress-induced reduction in the concentration of N-acetylaspartate, a putative marker of neuronal health, was prevented in the cortex and hippocampus. These findings suggest that paternal trauma can confer beneficial brain metabolism adaptations to acute stress in the offspring.
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Early-life stress-exposed mice show reductions in N-acetylaspartate in the frontal cortex and hypothalamus.
“These include reductions in N-acetylaspartate (a marker of neuronal integrity) in the frontal cortex and hypothalamus in early-life stress-exposed mice [97–99]”
From Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy (2024) · cites this paper as [97]
Cites
Subgenual prefrontal cortex abnormalities in mood disorders
Drevets, W. C., Price, J. L., Simpson, J. R., Todd, R. D., Reich, T., Vannier, M., & Raichle, M. E. (1997) · Nature · doi:10.1038/386824a0 · Cited by 2,693 · see citing works
Varese, F., Smeets, F., Drukker, M., Lieverse, R., Lataster, T., Viechtbauer, W., Read, J., van Os, J., & Bentall, R. P. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs050 · Cited by 2,436 · see citing works
Green, J. G., McLaughlin, K. A., Berglund, P. A., Gruber, M. J., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.186 · Cited by 2,323 · see citing works
Epigenetic transmission of the impact of early stress across generations
Franklin, T. B., Russig, H., Weiss, I. C., Gräff, J., Linder, N., Michalon, A., Vizi, S., & Mansuy, I. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.05.036 · Cited by 1,125 · cited 1× · see citing works
“For MSUS, dams and litters were subjected to 3-h daily separation unpredictably, during which dams were randomly and unpredictably exposed to restraint stress for 20min or forced swim stress for 5min.(13) Control mice were left undisturbed except for weekly cage changing.”
MethodSelf-citationJohnstone, T., van Reekum, C. M., Urry, H. L., Kalin, N. H., & Davidson, R. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2063-07.2007 · Cited by 1,051 · see citing works
Heim, C., & Binder, E. B. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.10.032 · Cited by 986 · see citing works
Izquierdo, A., Wellman, C. L., & Holmes, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0474-06.2006 · Cited by 459 · see citing works
Relationship of childhood maltreatment to the onset and course of major depression in adulthood
Bernet, C. Z., & Stein, M. B. (1999) · Depression and Anxiety · doi:10.1002/(sici)1520-6394(1999)9:4 · Cited by 289 · see citing works
Localized short‐echo‐time proton MR spectroscopy with full signal‐intensity acquisition
Mlynárik, V., Gambarota, G., Hanne Frenkel, A., & Rolf Gruetter, A. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21043 · Cited by 275 · see citing works
The epigenetics of social adversity in early life: Implications for mental health outcomes
McGowan, P. O., & Szyf, M. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.12.026 · Cited by 272 · see citing works
MR Spectroscopic Studies of the Brain in Psychiatric Disorders
Maddock, R. J., & Buonocore, M. H. (2011) · Current topics in behavioral neurosciences · doi:10.1007/7854_2011_197 · Cited by 266 · see citing works
Steen, R. G., Hamer, R. M., & Lieberman, J. A. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300850 · Cited by 254 · see citing works
The neurochemical profile quantified by in vivo 1H NMR spectroscopy
Duarte, J. M. N., Lei, H., Mlynárik, V., & Rolf Gruetter, A. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.12.038 · Cited by 222 · see citing works
Self-citationInfluence of Early Stress on Social Abilities and Serotonergic Functions across Generations in Mice
Franklin, T. B., Linder, N., Russig, H., Thöny, B., & Mansuy, I. M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021842 · Cited by 207 · see citing works
Self-citationAssaf, Y., & Cohen, Y. (2000) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(200002)43:2 · Cited by 184 · see citing works
Epigenetic Inheritance of Disease and Disease Risk
Bohacek, J., & Mansuy, I. M. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2012.110 · Cited by 176 · see citing works
Self-citationEffects of Dietary Sphingomyelin on Central Nervous System Myelination in Developing Rats
Oshida, K., Shimizu, T., Takase, M., Tamura, Y., Shimizu, T., & Yamashiro, Y. (2003) · Pediatric Research · doi:10.1203/01.pdr.0000054654.73826.ac · Cited by 171 · see citing works
Early life stress in fathers improves behavioural flexibility in their offspring
Gapp, K., Soldado-Magraner, S., Álvarez-Sánchez, M., Bohacek, J., Vernaz, G., Shu, H., Franklin, T. B., Wolfer, D. P., & Mansuy, I. M. (2014) · Nature Communications · doi:10.1038/ncomms6466 · Cited by 170 · see citing works
Self-citationInheritable Effect of Unpredictable Maternal Separation on Behavioral Responses in Mice
Weiss, I. C., Franklin, T. B., Vizi, S., & Mansuy, I. M. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00003 · Cited by 169 · see citing works
Self-citationJawahar, M. C., Murgatroyd, C., Harrison, E. L., & Baune, B. T. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0156-3 · Cited by 165 · see citing works
Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice
Gracia-Rubio, I., Moscoso-Castro, M., Pozo, O. J., Marcos, J., Nadal, R., & Valverde, O. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.09.003 · Cited by 144 · see citing works
Holland, F. H., Ganguly, P., Potter, D. N., Chartoff, E. H., & Brenhouse, H. C. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.02.023 · Cited by 125 · see citing works
Nonsteroidal Anti-Inflammatory Treatment Prevents Delayed Effects of Early Life Stress in Rats
Brenhouse, H. C., & Andersen, S. L. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.05.006 · Cited by 123 · see citing works
Disturbance of the Glutamatergic System in Mood Disorders
Jun, C. S., Choi, Y., Lim, S. M., Bae, S., Hong, Y. S., Kim, J. E., & Lyoo, I. K. (2014) · Experimental Neurobiology · doi:10.5607/en.2014.23.1.28 · Cited by 118 · see citing works
Maras, P. M., Molet, J., Chen, Y., Rice, C., Ji, S. G., Solodkin, A., & Baram, T. Z. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.12 · Cited by 118 · see citing works
Naaijen, J., Lythgoe, D. J., Amiri, H., Buitelaar, J. K., & Glennon, J. C. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.02.009 · Cited by 117 · see citing works
The Long-Term Impact of Early Adversity on Late-Life Psychiatric Disorders
Gershon, A., Sudheimer, K. D., Tirouvanziam, R. M., Williams, L. M., & O'Hara, R. M. (2013) · Current Psychiatry Reports · doi:10.1007/s11920-013-0352-9 · Cited by 112 · see citing works
Bohacek, J., Farinelli, M., Mirante, O., Steiner, G., Gapp, K., Coiret, G., Ebeling, M., Durán-Pacheco, G., Iniguez, A. L., Manuella, F., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.80 · Cited by 111 · see citing works
Self-citationDuarte, J. M. N., Kim, Q., & Rolf Gruetter, A. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.01.135 · Cited by 108 · see citing works
Self-citationToward understanding the impact of trauma on the early developing human brain
Thomason, M. E., & Marusak, H. A. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2016.02.022 · Cited by 101 · see citing works
The neuroenergetics of stress hormones in the hippocampus and implications for memory
Osborne, D. M., Pearson-Leary, J., & McNay, E. C. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00164 · Cited by 78 · see citing works
Wijtenburg, S. A., Yang, S., Fischer, B. A., & Rowland, L. M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.01.007 · Cited by 78 · see citing works
Shrira, A., Palgi, Y., Ben‐Ezra, M., & Shmotkin, D. (2011) · Psychological Trauma Theory Research Practice and Policy · doi:10.1037/a0020608 · Cited by 75 · see citing works
The oxidized form of vitamin C, dehydroascorbic acid, regulates neuronal energy metabolism
Cisternas, P., Silva-Álvarez, C., Martínez, F., Fernández, E., Ferrada, L., Oyarce, K., Salazar, K., Bolaños, J. P., & Nualart, F. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12663 · Cited by 74 · see citing works
Effects of stress and exercise on rat hippocampus and striatum extracellular lactate
Bruin, L. A. D., Schasfoort, E. M. C., Steffens, A. B., & Korf, J. (1990) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1990.259.4.r773 · Cited by 71 · see citing works
Paslakis, G., Träber, F., Roberz, J., Block, W., & Jessen, F. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2014.06.004 · Cited by 69 · see citing works
Goldstein, L. E., Rasmusson, A. M., Bunney, B., & Rh, R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-08-04937.1994 · Cited by 65 · see citing works
Metabolic Flux and Compartmentation Analysis in the Brain In vivo
Lanz, B., Rolf Gruetter, A., & Duarte, J. M. N. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00156 · Cited by 58 · see citing works
Self-citationMorrow, B. A., Clark, W. A., & Roth, R. H. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90855-c · Cited by 57 · see citing works
The C57BL/6J Mouse Exhibits Sporadic Congenital Portosystemic Shunts
Cudalbu, C., McLin, V. A., Lei, H., Duarte, J. M. N., Rougemont, A., Oldani, G., Terraz, S., Toso, C., & Rolf Gruetter, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069782 · Cited by 56 · see citing works
Self-citationMetabolic Disturbances in Diseases with Neurological Involvement
Duarte, J. M. N. (2014) · Aging and Disease · doi:10.14336/ad.2014.0500238 · Cited by 55 · see citing works
Self-citationHippocampal gene expression induced by cold swim stress depends on sex and handling
Bohacek, J., Manuella, F., Roszkowski, M., & Mansuy, I. M. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.10.026 · Cited by 51 · see citing works
Self-citationSalling, M. C., & Harrison, N. L. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00714.2013 · Cited by 50 · see citing works
Swim Stress Increases the Potency of Glycine at the N‐Methyl‐ d ‐Aspartate Receptor Complex
Nowak, G., Redmond, A., McNamara, M. G., & Paul, I. A. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.64020925.x · Cited by 43 · see citing works
Duarte, J. M. N., Girault, F., & Rolf Gruetter, A. (2014) · Journal of Neuroscience Research · doi:10.1002/jnr.23531 · Cited by 27 · see citing works
Self-citationNovel hypoglycemic injury mechanism: N‐methyl‐D‐aspartate receptor–mediated white matter damage
Yang, X., Hamner, M. A., Brown, A. M., Evans, R. D., Ye, Z., Chen, S., & Ransom, B. R. (2013) · Annals of Neurology · doi:10.1002/ana.24050 · Cited by 26 · see citing works
Zhang, J., Abdallah, C. G., Chen, Y., Huang, T., Huang, Q., Chong-tao, X., Xiao, Y., Liu, Y., Ding, Y., & Wu, R. (2013) · Neuroscience Letters · doi:10.1016/j.neulet.2013.04.035 · Cited by 24 · see citing works
Zhou, I. Y., Ding, A. Y., Li, Q., McAlonan, G. M., & Wu, E. X. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2012.09.010 · Cited by 22 · see citing works
Habituation of lactate release responding to stressful stimuli in rat prefrontal cortex in vivo
Takita, M., Mikuni, M., & Takahashi, K. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.3.r722 · Cited by 20 · see citing works
Liu, W., Shu, X., Chen, F.-Y., Zhu, C., Sun, X.-H., Liú, L., Ai, Y.-X., Li, Y., & Zhao, H. (2011) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.02.007 · Cited by 19 · see citing works
Kim, S.-Y., Jang, E.-J., Hong, K. S., Lee, C., Lee, D., Choi, C., Lee, H.-S., & Choe, B. (2011) · Neurochemical Research · doi:10.1007/s11064-011-0668-y · Cited by 14 · see citing works
Glycine receptor-mediated inhibition of medial prefrontal cortical pyramidal cells
Liu, Y., Huang, D. F., Wen, R., Chen, X., & Yi, H. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.12.014 · Cited by 7 · see citing works
Integrative Approaches for Lipid Analysis
Wang, Y., Li, M., & Fan, P. (2015) · Pharmacologia · doi:10.5567/pharmacologia.2015.213.234 · Cited by 4 · see citing works
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Gapp, K., van Steenwyk, G., Germain, P. L., Matsushima, W., Rudolph, K. L. M., Manuella, F., Roszkowski, M., Vernaz, G., Ghosh, T., Pelczar, P., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-018-0271-6 · Cited by 195 · see citing works
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Self-citationLizarbe, B., Soares, A. F., Larsson, S., & Duarte, J. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00985 · Cited by 123 · see citing works
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“…include reductions in N-acetylaspartate (a marker of neuronal integrity) in the frontal cortex and hypothalamus in early-life stress-exposed mice [97 – 99] and altered neurotransmitter metabolism of gamma-aminobutyric acid and glutamate in the right hippocampus of pre-gestational stress-exposed…”
Backgroundvan Steenwyk, G., Roszkowski, M., Manuella, F., Franklin, T. B., & Mansuy, I. M. (2018) · Environmental Epigenetics · doi:10.1093/eep/dvy023 · Cited by 116 · see citing works
Self-citationRafiee, Z., García-Serrano, A. M., & Duarte, J. M. N. (2022) · Nutrients · doi:10.3390/nu14061292 · Cited by 100 · see citing works
Self-citationDuarte, J. M. N., & Xin, L. (2018) · Neurochemical Research · doi:10.1007/s11064-018-2521-z · Cited by 69 · see citing works
Self-citationMitochondria and the Brain: Bioenergetics and Beyond
Belenguer, P., Duarte, J. M. N., Schuck, P. F., & Ferreira, G. C. (2019) · Neurotoxicity Research · doi:10.1007/s12640-019-00061-7 · Cited by 65 · see citing works
Self-citationGarcia-Serrano, A. M., Mohr, A. A., Philippe, J., Skoug, C., Spégel, P., & Duarte, J. M. N. (2022) · Aging and disease · doi:10.14336/ad.2021.0720 · Cited by 55 · see citing works
Self-citationInvolvement of circulating factors in the transmission of paternal experiences through the germline
van Steenwyk, G., Gapp, K., Jawaid, A., Germain, P., Manuella, F., Tanwar, D. K., Zamboni, N., Gaur, N., Efimova, A., Thumfart, K. M., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2020104579 · Cited by 48 · see citing works
Self-citationFrasch, M. G., Lobmaier, S. M., Stampalija, T., Desplats, P., Pallarés, M. E., Pastor, V. E., Brocco, M. A., Wu, H., Schulkin, J. A., Herry, C. L., et al. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.026 · Cited by 43 · see citing works
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Boscardin, C., Manuella, F., & Mansuy, I. M. (2022) · Current Zoology · doi:10.1093/eep/dvac024 · Cited by 29 · see citing works
Self-citationHe, Z.-X., Guo, Q.-Q., Yang, Y., Wang, L.-M., Zhang, S., Yuan, W., Li, L.-F., Zhang, J., Hou, W.-J., Yang, J., et al. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.09.006 · Cited by 25 · see citing works
Ferreira, H., Sousa, A. C., Sereno, J., Martins, J., Castelo-Branco, M. S., & Gonçalves, J. (2022) · Metabolites · doi:10.3390/metabo12010071 · Cited by 23 · see citing works
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Jawaid, A., & Mansuy, I. M. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.12.004 · Cited by 21 · see citing works
Self-citationCorcoba, A., Rolf Gruetter, A., Kim, Q., & Duarte, J. M. N. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14116 · Cited by 17 · see citing works
Self-citationLim, S., Song, K.-H., Yoo, C., Woo, D., & Choe, B. (2017) · Neurochemical Research · doi:10.1007/s11064-017-2232-x · Cited by 17 · see citing works
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Tan, X., Luo, J., Ding, X., & Li, H. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104976 · Cited by 15 · see citing works
Baram, T. Z., & Birnie, M. T. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100669 · Cited by 16 · see citing works
Sekar, S., Grandjean, J., Garnell, J. F., Willems, R., Duytschaever, H., Seramani, S., Huang, S., Donck, L. V., & Bhakoo, K. K. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.11.021 · Cited by 11 · see citing works
Tissue-specific epigenetic inheritance after paternal heat exposure in male wild guinea pigs
Weyrich, A., Yasar, S., Lenz, D., & Fickel, J. (2020) · Mammalian Genome · doi:10.1007/s00335-020-09832-6 · Cited by 11 · see citing works
Dad's legacy: Epigenetic reprogramming and paternal inflammatory memory in offspring health
Alipoor, S. D., Norouzitallab, P., Öst, A., & Lerm, M. (2025) · Journal of Internal Medicine · doi:10.1111/joim.20094 · Cited by 9 · see citing works
Liu, Y., Hou, J., Qi, Z., Yang, L., Du, Z., Wu, Y., Song, Q., Li, X., Sun, J., Chen, P., et al. (2025) · BMC Psychology · doi:10.1186/s40359-025-03088-y · Cited by 10 · see citing works
Jawaid, A., Gomolka, M., Tomaszewska, W., Kunzi, M., Mansoor, M., Przybys, J., Gbadamosi, I., Maloburska, A., Khan, Z. Y., Hidayat, T., et al. (2020) · medRxiv · doi:10.1101/2020.08.11.20168393 · Cited by 8 · see citing works
Self-citationCsaba, G. (2019) · Current Genomics · doi:10.2174/1389202920666191116113524 · Cited by 8 · see citing works
Differential susceptibility of male and female germ cells to glucocorticoid-mediated signaling
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Chiappelli, J., Savransky, A., Ma, Y., Gao, S., Kvarta, M. D., Kochunov, P. V., Slavich, G. M., & Hong, L. E. (2024) · Schizophrenia Research · doi:10.1016/j.schres.2024.04.027 · Cited by 5 · see citing works
Meknatkhah, S., Dashti, P. S., Raminfard, S., Rad, H. S., Mousavi, M., & Riazi, G. H. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01702-9 · Cited by 5 · see citing works
van Steenwyk, G., Gapp, K., Jawaid, A., Germain, P., Manuella, F., Tanwar, D. K., Zamboni, N., Gaur, N., Efimova, A., Thumfart, K. M., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/653865 · Cited by 5 · see citing works
Self-citationHwang, Y. H., Lee, M., Yun, C., Kim, Y., Baek, H., Han, B. S., & Kim, D. Y. (2021) · Journal of Spectroscopy · doi:10.1155/2021/6533727 · Cited by 4 · see citing works
Dehkordi, O., Lin, S., Mohamud, S., Millis, R. M., & Wang, P. C. (2025) · Current Research in Physiology · doi:10.1016/j.crphys.2025.100147 · Cited by 2 · see citing works
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Differential susceptibility of male and female germ cells to glucocorticoid-mediated signaling
Cincotta, S. A., Richardson, N., Foecke, M. H., & Laird, D. J. (2024) · eLife · doi:10.7554/elife.90164.3 · Cited by 2 · see citing works
Duarte, J. M. N. (2025) · Neurochemical Research · doi:10.1007/s11064-024-04324-4 · Cited by 2 · see citing works
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Barokah, A. N., Gürsoy, İ., Dönmez, M. H., Fitremann, J., Bayramov, R., & Bayram, K. K. (2026) · Neurochemical Research · doi:10.1007/s11064-026-04822-7 · Cited by 1 · see citing works
Epigenetic Inheritance and the Environment
Jablonka, E. (2024) · Springer eBooks · doi:10.1007/978-3-031-61187-2_5 · Cited by 1 · see citing works
Dehkordi, O., Lin, S., Mohamud, S., Millis, R. M., & Wang, P. C. (2025) · Cureus · doi:10.7759/cureus.79972 · Cited by 1 · see citing works
Just, N. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.14.203067
Differential susceptibility of male and female germ cells to glucocorticoid-mediated signalingPreprint
Cincotta, S. A., Richardson, N., Foecke, M. H., & Laird, D. J. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.30.547215
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Cincotta, S. A., Richardson, N., Foecke, M. H., & Laird, D. J. (2023) · eLife · doi:10.7554/elife.90164.2
Role of GIRK2 channels in morphine-induced metabolite changes in the rostral ventromedial medulla
Dehkordi, O., Lin, S., Mohamud, S., Dávila‐García, M. I., Millis, R. M., & Wang, P. C. (2026) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2026.110668
da Silva, B. R. D., Nunes, P. I. G., de Matos, R. S., Silva, L. M. A., FILHO, E. D. G. A., de Brito, E. S., de Bruin, P. F. C., & de Bruin, V. M. S. (2026) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x2025e14816
- Authors
- Gapp, K., Corcoba, A., van Steenwyk, G., Mansuy, I. M., & Duarte, J. M.
- Affiliations
- University of Zurich (CH)
- École Polytechnique Fédérale de Lausanne (CH)
- Laboratory of Neuroepigenetics, University of Zurich and Swiss Federal Institute of Technology, Zürich, Switzerland
- Corresponding author
- Duarte, João MN
- Venue
- Journal of Cerebral Blood Flow & Metabolism
- Publisher
- SAGE Publications
- Published
- 2016-10-01
- Volume
- 37
- Issue
- 7
- Pages
- 2423-2432
- ISSN
- 0271-678X (ISSN-L)
- 1559-7016
- PMC
- PMC5531341
- OpenAlex
- W2516097749
- Cited by
- 48
- References
- 53
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 5 · 2023: 4 · 2022: 5 · 2021: 2 · 2020: 7 · 2019: 5 · 2018: 9 · 2017: 2
- FWCI
- 3.38
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Lund University Publications (Lund University) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- École Polytechnique Fédérale de Lausanne
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (148250)
- Centre d'Imagerie BioMédicale
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- early life stress, traumatic stress, transgenerational transmission, brain metabolism, neurochemical profile, N-acetylaspartate, glutamate, GABA, prefrontal cortex, hippocampus, striatum, acute stress response, neuronal dysfunction
- MeSH terms
- Animals, Animals, Newborn, Brain, Brain Chemistry, Cerebral Cortex, Corpus Striatum, Female, Hippocampus, Male, Maternal Deprivation, Mice, Inbred C57BL, Magnetic Resonance Spectroscopy, Pregnancy, Prenatal Exposure Delayed Effects, Restraint, Physical, Stress, Psychological, Swimming
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