Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice

Gracia-Rubio, Irene; Moscoso-Castro, Maria; Pozo, Oscar J.; Marcos, Josep; Nadal, Roser; Valverde, Olga

doi:10.1016/j.pnpbp.2015.09.003

Cited by 144Tryptophan and brain disordersStress Responses and CortisolNeuroinflammation and Neurodegeneration Mechanisms

Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice

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Gracia-Rubio, Irene, Moscoso-Castro, Maria, Pozo, Oscar J., Marcos, Josep, Nadal, Roser, Valverde, Olga·2016·Progress in Neuro-Psychopharmacology and Biological Psychiatry

DOI 10.1016/j.pnpbp.2015.09.003

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Abstract

Early life experiences play a key role in brain function and behaviour. Adverse events during childhood are therefore a risk factor for psychiatric disease during adulthood, such as mood disorders. Maternal separation is a validated mouse model for maternal neglect, producing negative early life experiences that result in subsequent emotional alteration. Mood disorders have been found to be associated with neurochemical changes and neurotransmitter deficits such as reduced availability of monoamines in discrete brain areas. Emotional alterations like depression result in reduced serotonin availability and enhanced kynurenine metabolism through the action of indoleamine 2, 3-dioxygenase in response to neuroinflammatory factors. This mechanism involves regulation of the neurotransmitter system by neuroinflammatory agents, linking mood regulation to neuroinmunological reactions. In this context, the aim of this study was to investigate the effects of maternal separation with early weaning on emotional behaviour in mice. We investigated neuroinflammatory responses and the state of the tryptophan-kynurenine metabolic pathway in discrete brain areas following maternal separation. We show that adverse events during early life increase risk of long-lasting emotional alterations during adolescence and adulthood. These emotional alterations are particularly severe in females. Behavioural impairments were associated with microglia activation and disturbed tryptophan-kynurenine metabolism in brain areas related to emotional control. This finding supports the preeminent role of neuroinflammation in emotional disorders.

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Early adversity, including maternal separation and early infection, during infancy results in larger, activated microglia in rodents.
“In particular, rodent studies have demonstrated that early adversity, including maternal separation and early infection, during infancy results in larger, activated microglia, resident immune cells in the brain that secrete inflammatory cytokines (Bilbo, 2013; Gracia-Rubio et al., 2015).”
From Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease (2017) · cites this paper as Gracia-Rubio et al., 2015

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Litter size affects emotionality in adult male rats
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Clinical and Neuroradiologic Features Associated With Chronicity in Late-Life Depression
Lavretsky, H., Lesser, I. M., Wohl, M. A., Miller, B. L., & Mehringer, C. M. (1999) · American Journal of Geriatric Psychiatry · doi:10.1097/00019442-199911000-00006 · Cited by 69 · see citing works
Evidence for a key role of the peripheral kynurenine pathway in the modulation of anxiety- and depression-like behaviours in mice: Focus on individual differences
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Regulation of Hippocampal cGMP Levels as a Candidate to Treat Cognitive Deficits in Huntington’s Disease
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Estrogen Action in Mood and Neurodegenerative Disorders: Estrogenic Compounds with Selective Properties–The Next Generation of Therapeutics
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Individual differences in anhedonic and accumbal dopamine responses to chronic social stress and their link to cocaine self-administration in female rats
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α7 Nicotinic Acetylcholine Receptor-Specific Antibody Induces Inflammation and Amyloid β42 Accumulation in the Mouse Brain to Impair Memory
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THC Prevents MDMA Neurotoxicity in Mice
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Maternal neglect with reduced depressive-like behavior and blunted c-fos activation in Brattleboro mothers, the role of central vasopressin
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Anxiolytic actions of diazepam, but not of buspirone, are influenced by gender and the endocrine stage
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Sex-dependent effects of an early life treatment in rats that increases maternal care: vulnerability or resilience?
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Modulation of Passive Avoidance in Mice by the 5-HT1A Receptor Agonist Flesinoxan: Comparison with the Benzodiazepine Receptor Agonist Diazepam
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A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice
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The differential effects of prenatal stress in rats on the acoustic startle reflex under baseline conditions and in response to anxiogenic drugs
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No Relationship between Sequence Variation in Protein Coding Regions of the Tas1r3 Gene and Saccharin Preference in Rats
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Behavioural and neuroinflammatory effects of the combination of binge ethanol and MDMA in mice
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Estrous cycle and sex affect cocaine-induced behavioural changes in CD1 mice
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Dizocilpine prevents the enhanced locomotor response to quinpirole induced by repeated electroconvulsive shock
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Maternal-infant separation impedes changes in feeding behavior during estrous cycle of rats
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Microglia, Lifestyle Stress, and Neurodegeneration
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Role of the Kynurenine Metabolism Pathway in Inflammation-Induced Depression: Preclinical Approaches
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Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease
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“In particular, rodent studies have demonstrated that early adversity, including maternal separation and early infection, during infancy results in larger, activated microglia, resident immune cells in the brain that secrete inflammatory cytokines (Bilbo, 2013; Gracia-Rubio et al., 2015).”
Bifidobacterium CECT 7765 modulates early stress-induced immune, neuroendocrine and behavioral alterations in mice
Moya-Pérez, Á., Pérez‐Villalba, A., Benítez‐Páez, A., Campillo, I., & Sanz, Y. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.05.011 · Cited by 177 · see citing works
Stress-related regulation of the kynurenine pathway: Relevance to neuropsychiatric and degenerative disorders
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Reconceptualization of translocator protein as a biomarker of neuroinflammation in psychiatry
Notter, T., Coughlin, J. M., Sawa, A., & Meyer, U. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.232 · Cited by 142 · see citing works
Repeated Cannabidiol treatment reduces cocaine intake and modulates neural proliferation and CB1R expression in the mouse hippocampus
Luján, M. Á., Castro‐Zavala, A., Alegre-Zurano, L., & Valverde, O. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.09.043 · Cited by 130 · see citing works
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How Early Life Stress Impact Maternal Care: A Systematic Review of Rodent Studies
Orso, R., Creutzberg, K. C., Wearick‐Silva, L. E., Viola, T. W., Tractenberg, S. G., Benetti, F., & Grassi‐Oliveira, R. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00197 · Cited by 121 · see citing works
Minocycline inhibits microglial activation and alleviates depressive-like behaviors in male adolescent mice subjected to maternal separation
Han, Y., Zhang, L., Wang, Q., Zhang, D.-D., Zhao, Q., Zhang, J., Xie, L., Liu, G., & You, Z. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.04.021 · Cited by 105 · see citing works
Effects of Early-Life Stress on Social and Anxiety-Like Behaviors in Adult Mice: Sex-Specific Effects
Bondar, N. P., Lepeshko, A. A., & Reshetnikov, V. V. (2018) · Behavioural Neurology · doi:10.1155/2018/1538931 · Cited by 105 · see citing works
Targeting tryptophan and tyrosine metabolism by liquid chromatography tandem mass spectrometry
Marcos, J., Renau, N., Valverde, O., Laín, G. A., Gracia‐Rubio, I., González-Sepúlveda, M., Jurado, L. A. P., Ventura, R., Segura, J., & Pozo, Ó. J. (2016) · Journal of Chromatography A · doi:10.1016/j.chroma.2016.01.023 · Cited by 97 · see citing works
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Plasticity of the epigenome during early-life stress
Barnett-Burns, S., Szyszkowicz, J. K., Luheshi, G. N., Lutz, P.-É., & Turecki, G. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.09.033 · Cited by 91 · see citing works
The Influence of Adverse Childhood Experiences in Pain Management: Mechanisms, Processes, and Trauma-Informed Care
Tidmarsh, L. V., Harrison, R. N., Ravindran, D., Matthews, S. L., & Finlay, K. A. (2022) · Frontiers in Pain Research · doi:10.3389/fpain.2022.923866 · Cited by 89 · see citing works
Dynamic changes in hippocampal microglia contribute to depressive-like behavior induced by early social isolation
Gong, Y. L., Tong, L., Yang, R., Hu, W., Xu, X., Wang, W., Wang, P., Lu, X., Gao, M., Wu, Y. H., et al. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.03.023 · Cited by 87 · see citing works
Adolescent voluntary exercise attenuated hippocampal innate immunity responses and depressive-like behaviors following maternal separation stress in male rats
Sadeghi, M., Peeri, M., & Hosseini, M.-J. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.017 · Cited by 83 · see citing works
Neuroimmune Interactions in Schizophrenia: Focus on Vagus Nerve Stimulation and Activation of the Alpha-7 Nicotinic Acetylcholine Receptor
Zuelli, F. M. D. G. C., Brognara, F., Quirino, G. F. S., Hiroki, C. H., Fais, R. S., Del‐Ben, C. M., Ulloa, L., Salgado, H. C., Kanashiro, A., & Loureiro, C. M. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00618 · Cited by 69 · see citing works
Behavioral effects in adolescence and early adulthood in two length models of maternal separation in male rats
Banqueri, M., Méndez, M., & Arias, J. L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.02.006 · Cited by 62 · see citing works
Milk osteopontin promotes brain development by up‐regulating osteopontin in the brain in early life
Jiang, R., Prell, C., & Lönnerdal, B. L. (2018) · The FASEB Journal · doi:10.1096/fj.201701290rr · Cited by 60 · see citing works
The Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models
Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 52 · see citing works
Maternal separation increases alcohol-drinking behaviour and reduces endocannabinoid levels in the mouse striatum and prefrontal cortex
Portero-Tresserra, M., Gracia-Rubio, I., Cantacorps, L., Pozo, O. J., Gómez-Gómez, A., Pastor, A., López-Arnau, R., de la Torre, R., & Valverde, O. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.02.003 · Cited by 55 · see citing works
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The pharmacological reduction of hippocampal neurogenesis attenuates the protective effects of cannabidiol on cocaine voluntary intake
Luján, M. Á., Cantacorps, L., & Valverde, O. (2019) · Addiction Biology · doi:10.1111/adb.12778 · Cited by 54 · see citing works
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Comorbidity between Alzheimer’s disease and major depression: a behavioural and transcriptomic characterization study in mice
Martín‐Sánchez, A., Piñero, J., Nonell, L., Arnal, M., Ribé, E. M., Nevado‐Holgado, A. J., Lovestone, S., Sanz, F., Furlong, L. I., & Valverde, O. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00810-x · Cited by 50 · see citing works
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Maternal separation in rodents: a journey from gut to brain and nutritional perspectives
Rincel, M., & Darnaudéry, M. (2019) · Proceedings of The Nutrition Society · doi:10.1017/s0029665119000958 · Cited by 50 · see citing works
Brain metabolic alterations in mice subjected to postnatal traumatic stress and in their offspring
Gapp, K., Corcoba, A., van Steenwyk, G., Mansuy, I. M., & Duarte, J. M. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16667525 · Cited by 48 · see citing works
Of bowels, brain and behavior: A role for the gut microbiota in psychiatric comorbidities in irritable bowel syndrome
Wilmes, L., Collins, J. M., O’Riordan, K. J., O’Mahony, S. M., Cryan, J. F., & Clarke, G. A. (2021) · Neurogastroenterology & Motility · doi:10.1111/nmo.14095 · Cited by 48 · see citing works
The burden of early life stress on the nociceptive system development and pain responses
Melchior, M., Kuhn, P., & Poisbeau, P. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15153 · Cited by 49 · see citing works
Adolescent escitalopram prevents the effects of maternal separation on depression‐ and anxiety‐like behaviours and regulates the levels of inflammatory cytokines in adult male mice
Wang, Q., Dong, X., Wang, Y., Liu, M., Sun, A., Li, N., Lin, Y., Geng, Z., Jin, Y., & Li, X. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.07.007 · Cited by 46 · see citing works
Long-term maternal separation potentiates depressive-like behaviours and neuroinflammation in adult male C57/BL6J mice
Zhou, L., Wu, Z., Wang, G., Xiao, L., Wang, H., Sun, L., & Xie, Y. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.172953 · Cited by 46 · see citing works
Ganoderma Lucidum Triterpenoids Improve Maternal Separation-Induced Anxiety- and Depression-like Behaviors in Mice by Mitigating Inflammation in the Periphery and Brain
Mi, X., Zeng, G., Liu, J., Luo, Z., Zhang, L., Dai, X., Fang, W., Zhang, J., & Chen, X. (2022) · Nutrients · doi:10.3390/nu14112268 · Cited by 46 · see citing works
Experiencing early life maternal separation increases pain sensitivity in adult offspring
Vilela, F. C., Vieira, J. S., Giusti‐Paiva, A., & da Silva, M. L. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.07.003 · Cited by 45 · see citing works
Aspects of Tryptophan and Nicotinamide Adenine Dinucleotide in Immunity: A New Twist in an Old Tale
Biefer, H. R. C., Vasudevan, A., & Elkhal, A. (2017) · International Journal of Tryptophan Research · doi:10.1177/1178646917713491 · Cited by 44 · see citing works
Adverse effects of early-life stress: focus on the rodent neuroendocrine system
Lee, S. H., & Jung, E. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.377587 · Cited by 43 · see citing works
The Effect of Early Maternal Separation Combined With Adolescent Chronic Unpredictable Mild Stress on Behavior and Synaptic Plasticity in Adult Female Rats
Huang, J., Shen, C., Ye, R., Shi, Y., & Li, W. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.539299 · Cited by 40 · see citing works
Socio-emotional challenges and development of children left behind by migrant mothers
Qu, X., Wang, X., Huang, X., Ashish, K. C., Yang, Y., Huang, Y., Chen, C., Gao, Y., Wang, Y., & Zhou, H. (2020) · Journal of Global Health · doi:10.7189/jogh.10.010806 · Cited by 40 · see citing works
Maternal Separation Impairs Cocaine-Induced Behavioural Sensitization in Adolescent Mice
Gracia‐Rubio, I., Laorden, E. M., Moscoso‐Castro, M., Milanés, M. V., Laorden, M. L., & Valverde, O. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167483 · Cited by 39 · see citing works
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Glucocorticoid programming of neuroimmune function
Walker, D. J., & Spencer, K. A. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.07.016 · Cited by 40 · see citing works
Maternal Separation Does Not Produce a Significant Behavioral Change in Mice
Tan, S., Ho, H. S., Song, A. Y., Low, J., & Je, H. S. (2017) · Experimental Neurobiology · doi:10.5607/en.2017.26.6.390 · Cited by 38 · see citing works
Basic Concept of Microglia Biology and Neuroinflammation in Relation to Psychiatry
Mattei, D., & Notter, T. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_83 · Cited by 37 · see citing works
Increasing kynurenine brain levels reduces ethanol consumption in mice by inhibiting dopamine release in nucleus accumbens
Giménez‐Gómez, P., Pérez‐Hernández, M., Gutiérrez‐López, M. D., Vidal, R., Abuin-Martínez, C., O’Shea, E., & Colado, M. I. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.04.016 · Cited by 37 · see citing works
The Epigenetics of Early Life Adversity: Current Limitations and Possible Solutions
Barnett-Burns, S., Almeida, D. M., & Turecki, G. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.01.008 · Cited by 34 · see citing works
Synergistic effects of early life mild adversity and chronic social defeat on rat brain microglia and cytokines
Ferle, V., Repouskou, A., Aspiotis, G., Raftogianni, A., Chrousos, G. P., Stylianopoulou, F., & Stamatakis, A. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112791 · Cited by 34 · see citing works
Curcumin treatment attenuates alcohol-induced alterations in a mouse model of foetal alcohol spectrum disorders
Cantacorps, L., Montagud‐Romero, S., & Valverde, O. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109899 · Cited by 33 · see citing works
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Cognitive impairments associated with alterations in synaptic proteins induced by the genetic loss of adenosine A 2A receptors in mice
Moscoso‐Castro, M., López‐Cano, M., Gracia‐Rubio, I., Ciruela, F., & Valverde, O. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.08.027 · Cited by 32 · see citing works
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Reconsidering depression as a risk factor for substance use disorder: Insights from rodent models
Rappeneau, V., & Bérod, A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.001 · Cited by 32 · see citing works
Early life stress increases vulnerability to the sequelae of pediatric mild traumatic brain injury
Díaz-Chávez, A., Lajud, N., Roque, A., B, J. P. C. A., Meléndez‐Herrera, E., Valdez-Alarcón, J. J., Bondi, C. O., & Kline, A. E. (2020) · Experimental Neurology · doi:10.1016/j.expneurol.2020.113318 · Cited by 31 · see citing works
Maternal separation as early-life stress: Mechanisms of neuropsychiatric disorders and inspiration for neonatal care
Zhang, Y., Wang, S., & Hei, M. (2024) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2024.111058 · Cited by 29 · see citing works
Sex differences in the vulnerability to cocaine's addictive effects after early-life stress in mice
Castro‐Zavala, A., Martín‐Sánchez, A., & Valverde, O. (2020) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2019.12.112 · Cited by 29 · see citing works
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Early life adversity drives sex-specific anhedonia and meningeal immune gene expression through mast cell activation
Duque‐Wilckens, N., Teis, R., Sarno, E., Stölting, F., Khalid, S., Dairi, Z., Douma, A., Maradiaga, N. C., Hench, S., Dharshika, C., et al. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.03.009 · Cited by 26 · see citing works
Sex-dependence and comorbidities of the early-life adversity induced mental and metabolic disease risks: Where are we at?
Reemst, K., Ruigrok, S. R., Bleker, L. S., Naninck, E. F. G., Ernst, T. R., Kotah, J. M., Lucassen, P. J., Roseboom, T. J., Pollux, B. J. A., de Rooij, S. R., et al. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104627 · Cited by 26 · see citing works
Maternal separation stress through triggering of the neuro‐immune response in the hippocampus induces autistic‐like behaviors in male mice
Reisi‐Vanani, V., Lorigooini, Z., Bijad, E., & Amini-Khoei, H. (2023) · International Journal of Developmental Neuroscience · doi:10.1002/jdn.10310 · Cited by 25 · see citing works
Early-life stress induces emotional and molecular alterations in female mice that are partially reversed by cannabidiol
Martín‐Sánchez, A., González‐Pardo, H., Alegre-Zurano, L., Castro‐Zavala, A., López-Taboada, I., Valverde, O., & Conejo, N. M. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2021.110508 · Cited by 25 · see citing works
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Long-term Effects of Maternal Separation on Anxiety-Like Behavior and Neuroendocrine Parameters in Adult Balb/c Mice
Kestering-Ferreira, É., Tractenberg, S. G., Lumertz, F. S., Orso, R., Creutzberg, K. C., Wearick‐Silva, L. E., Viola, T. W., & Grassi‐Oliveira, R. (2021) · Chronic Stress · doi:10.1177/24705470211067181 · Cited by 24 · see citing works
Early-life stress elicits peripheral and brain immune activation differently in wild type and 5xFAD mice in a sex-specific manner
Bachiller, S., Hidalgo, I., García, M. G., Boza-Serrano, A., Paulus, A., Denis, Q., Haikal, C., Manouchehrian, O., Klementieva, O., Li, J.-Y., et al. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02515-w · Cited by 25 · see citing works
Effects of oleanolic acid and ursolic acid on depression-like behaviors induced by maternal separation in mice
Kong, C. H., Park, K., Kim, D. Y., Kim, J. Y., Kang, W. C., Jeon, M., Min, J. W., Lee, W. H., Jung, S. Y., & Ryu, J. H. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.175954 · Cited by 23 · see citing works
Sex-dependent effects of paternal deprivation and chronic variable stress on novel object recognition in adult California mice (Peromyscus californicus)
Agarwal, P., Palin, N., Walker, S. L., & Glasper, E. R. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104610 · Cited by 23 · see citing works
Effects of fast-acting antidepressant drugs on a postpartum depression mice model
García-Baos, A., Gallego‐Landin, I., Ferreres-Álvarez, I., Puig-Reyné, X., Castro‐Zavala, A., Valverde, O., & Martín‐Sánchez, A. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113598 · Cited by 19 · see citing works
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Animal Models of the Impact of Social Stress on Cocaine Use Disorders
Vannan, A., Powell, G. L., Scott, S. N., Pagni, B. A., & Neisewander, J. L. (2018) · International review of neurobiology · doi:10.1016/bs.irn.2018.07.005 · Cited by 21 · see citing works
Chemogenetic manipulation of the bed nucleus of the stria terminalis counteracts social behavioral deficits induced by early life stress in C57BL/6J mice
Emmons, R., Sadok, T., Rovero, N. G., Belnap, M. A., Henderson, H. J. M., Quan, A., Toro, N. J. D., & Halladay, L. R. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24644 · Cited by 19 · see citing works
Maternal separation increases cocaine intake through a mechanism involving plasticity in glutamate signalling
Castro‐Zavala, A., Martín‐Sánchez, A., Luján, M. Á., & Valverde, O. (2020) · Addiction Biology · doi:10.1111/adb.12911 · Cited by 20 · see citing works
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Authors: Gracia-Rubio, I., Moscoso-Castro, M., Pozo, O. J., Marcos, J., Nadal, R., & Valverde, O.
Affiliations: Universitat Pompeu Fabra (ES)
Universitat Autònoma de Barcelona (ES)
Corresponding author: Valverde, Olga
ORCID: Marcos, Josep
Nadal, Roser
Valverde, Olga
Venue: Progress in Neuro-Psychopharmacology and Biological Psychiatry
Publisher: Elsevier BV
Published: 2016-02
Volume: 65
Pages: 104-117
ISSN: 0278-5846 (ISSN-L)
DOI: 10.1016/j.pnpbp.2015.09.003
OpenAlex: W1651663774
Cited by: 144
References: 113
Citations by year: 2026: 4 · 2025: 12 · 2024: 11 · 2023: 14 · 2022: 14 · 2021: 18 · 2020: 20 · 2019: 12 · 2018: 12 · 2017: 19 · 2016: 7 · 2015: 1
FWCI: 4.38
Type: journal article
Language: en
Open access: green
zaguan.unizar.es
Licence: cc-by-nc-nd
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Progress in Neuro-Psychopharmacology and Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Zaguan (University of Zaragoza Repository) (acceptedVersion, cc-by-nc-nd)
Funders: MINECO (SAF2013-41761-R-FEDER)
Ministry of Health (Retic-ISCIII-RD/12/0028/0014-FEDER, Retic-ISCIII-RD/12/0028/0024-FEDER)
Plan Nacional sobre Drogas (2014/020)
Generalitat de Catalunya (2014SGR692, 2014SGR34, 2014SGR1020)
FPI fellowship (BES-2011-046655, SAF2010-15793)
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: maternal separation, neuroinflammation, childhood adversity, maternal neglect, emotional behavior, depression, tryptophan-kynurenine metabolism, microglial activation, indoleamine 2,3-dioxygenase, serotonin, kynurenine, monoamines, sex differences, mood disorders, adolescence, mice
MeSH terms: Animals, Avoidance Learning, Body Weight, Brain, Disease Models, Animal, Emotions, Exploratory Behavior, Female, Kynurenine, Male, Maternal Behavior, Maternal Deprivation, Motor Activity, Random Allocation, Neuroimmunomodulation, Pain Threshold, Mice

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Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice

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