Cited by 204Neuroinflammation and Neurodegeneration MechanismsStress Responses and CortisolNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 56 of the 56 references it cites were found in a registry or an index.

Neuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat

Open access

McKim, Daniel B., Niraula, Anzela, Tarr, Andrew J., Wohleb, Eric S., Sheridan, John F., Godbout, Jonathan P.·2016·The Journal of Neuroscience

DOI 10.1523/jneurosci.2394-15.2016PMC PMC4879207

Open this paper in CoChat — free account

Abstract

Repeated social defeat (RSD) is a murine stressor that recapitulates key physiological, immunological, and behavioral alterations observed in humans exposed to chronic psychosocial stress. Psychosocial stress promotes prolonged behavioral adaptations that are associated with neuroinflammatory signaling and impaired neuroplasticity. Here, we show that RSD promoted hippocampal neuroinflammatory activation that was characterized by proinflammatory gene expression and by microglia activation and monocyte trafficking that was particularly pronounced within the caudal extent of the hippocampus. Because the hippocampus is a key area involved in neuroplasticity, behavior, and cognition, we hypothesize that stress-induced neuroinflammation impairs hippocampal neurogenesis and promotes cognitive and affective behavioral deficits. We show here that RSD caused transient impairments in spatial memory recall that resolved within 28 d. In assessment of neurogenesis, the number of proliferating neural progenitor cells (NPCs) and the number of young, developing neurons were not affected initially after RSD. Nonetheless, the neuronal differentiation of NPCs that proliferated during RSD was significantly impaired when examined 10 and 28 d later. In addition, social avoidance, a measure of depressive-like behavior associated with caudal hippocampal circuitry, persisted 28 d after RSD. Treatment with minocycline during RSD prevented both microglia activation and monocyte recruitment. Inhibition of this neuroinflammatory activation in turn prevented impairments in spatial memory after RSD but did not prevent deficits in neurogenesis nor did it prevent the persistence of social avoidance behavior. These findings show that neuroinflammatory activation after psychosocial stress impairs spatial memory performance independent of deficits in neurogenesis and social avoidance. SIGNIFICANCE STATEMENT Repeated exposure to stress alters the homeostatic environment of the brain, giving rise to various cognitive and mood disorders that impair everyday functioning and overall quality of life. The brain, previously thought of as an immune-privileged organ, is now known to communicate extensively with the peripheral immune system. This brain–body communication plays a significant role in various stress-induced inflammatory conditions, also characterized by psychological impairments. Findings from this study implicate neuroimmune activation rather than impaired neurogenesis in stress-induced cognitive deficits. This idea opens up possibilities for novel immune interventions in the treatment of cognitive and mood disturbances, while also adding to the complexity surrounding the functional implications of adult neurogenesis.

Integrity signals

Registry

Crossref · 10.1523/jneurosci.2394-15.2016

Cites

56 of 56 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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 Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859
Copper-Zinc Superoxide Dismutase (SOD1) Is Released by Microglial Cells and Confers Neuroprotection against 6-OHDA Neurotoxicity
Polazzi, E., Mengoni, I., Caprini, M., Peña‐Altamira, E., Kurtys, E., & Monti, B. (2012) · Neurosignals · doi:10.1159/000337115 · Cited by 9,023
Glutamate neurotoxicity and diseases of the nervous system
Choi, D. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90162-6 · Cited by 8,188
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180
Inflammation and Its Discontents: The Role of Cytokines in the Pathophysiology of Major Depression
Miller, A. H., Maletic, V., & Raison, C. L. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.11.029 · Cited by 3,848
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
Spatial localization does not require the presence of local cues
Morris, R. G. M. (1981) · Learning and Motivation · doi:10.1016/0023-9690(81)90020-5 · Cited by 2,699
Molecular Adaptations Underlying Susceptibility and Resistance to Social Defeat in Brain Reward Regions
Krishnan, V., Han, M.-H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., LaPlant, Q., Graham, A., Lutter, M., Lagace, D. C., et al. (2007) · Cell · doi:10.1016/j.cell.2007.09.018 · Cited by 2,307
Stress-induced immune dysfunction: implications for health
Glaser, R., & Kiecolt-Glaser, J. K. (2005) · Nature Reviews Immunology · doi:10.1038/nri1571 · Cited by 2,190
Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress
Berton, O., McClung, C. A., DiLeone, R. J., Krishnan, V., Renthal, W., Russo, S. J., Graham, D., Tsankova, N. M., Bolanos, C. A., Rios, M., et al. (2006) · Science · doi:10.1126/science.1120972 · Cited by 2,129

Show all 56 references

Sorted by citations

Integrating neuroimmune systems in the neurobiology of depression
Wohleb, E. S., Franklin, T., Iwata, M., & Duman, R. S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.69 · Cited by 668
Self-citation
Microglia Priming with Aging and Stress
Niraula, A., Sheridan, J. F., & Godbout, J. P. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.185 · Cited by 398
Self-citation
Microglial recruitment of IL-1β-producing monocytes to brain endothelium causes stress-induced anxiety
McKim, D. B., Weber, M. D., Niraula, A., Sawicki, C. M., Liu, X., Jarrett, B. L., Ramirez-Chan, K., Wang, Y., Roeth, R. M., Sucaldito, A. D., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.64 · Cited by 365
Self-citation
Neuroinflammation, memory, and depression: new approaches to hippocampal neurogenesis
Wu, A., & Zhang, J. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02964-x · Cited by 354
Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal
Weber, M. D., Godbout, J. P., & Sheridan, J. F. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2016.102 · Cited by 283
Self-citation
The Cholinergic System Modulates Memory and Hippocampal Plasticity via Its Interactions with Non-Neuronal Cells
Maurer, S. V., & Williams, C. L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01489 · Cited by 276
Microglia Play an Active Role in Obesity-Associated Cognitive Decline
Cope, E. C., LaMarca, E. A., Monari, P. K., Olson, L. B., Martinez, S., Zych, A. D., Katchur, N. J., & Gould, E. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0789-18.2018 · Cited by 219
Neuron–Microglia Interactions in Mental Health Disorders: “For Better, and For Worse”
Wohleb, E. S. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00544 · Cited by 170
Self-citation
Gene deficiency and pharmacological inhibition of caspase-1 confers resilience to chronic social defeat stress via regulating the stability of surface AMPARs
Li, M., Zheng, H.-L., Luo, Y., He, J.-G., Wang, W., Han, J., Zhang, L., Wang, X., Ni, L., Zhou, H.-Y., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.76 · Cited by 163
Social Stress Mobilizes Hematopoietic Stem Cells to Establish Persistent Splenic Myelopoiesis
McKim, D. B., Yin, W., Wang, Y., Cole, S. W., Godbout, J. P., & Sheridan, J. F. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.102 · Cited by 153
Self-citation
Corticosterone Production during Repeated Social Defeat Causes Monocyte Mobilization from the Bone Marrow, Glucocorticoid Resistance, and Neurovascular Adhesion Molecule Expression
Niraula, A., Wang, Y., Godbout, J. P., & Sheridan, J. F. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.2568-17.2018 · Cited by 137
Self-citation
Microglial Over-Activation by Social Defeat Stress Contributes to Anxiety- and Depressive-Like Behaviors
Stein, D. J., Vasconcelos, M., Albrechet‐Souza, L., Ceresér, K. M., & de Almeida, R. M. M. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00207 · Cited by 137
Neuroendocrine Regulation of Brain Cytokines After Psychological Stress
Johnson, J. D., Barnard, D. F., Kulp, A. C., & Mehta, D. M. (2019) · Journal of the Endocrine Society · doi:10.1210/js.2019-00053 · Cited by 135
Role of the adipose PPARγ-adiponectin axis in susceptibility to stress and depression/anxiety-related behaviors
Guo, M., Li, C., Lei, Y., Xu, S., Zhao, D., & Lu, X.-Y. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.225 · Cited by 130
The neuroimmunology of social-stress-induced sensitization
Biltz, R. G., Sawicki, C. M., Sheridan, J. F., & Godbout, J. P. (2022) · Nature Immunology · doi:10.1038/s41590-022-01321-z · Cited by 132
Self-citation
Brain-spleen axis in health and diseases: A review and future perspective
Wei, Y., Wang, T., Liao, L., Fan, X., Chang, L., & Hashimoto, K. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.02.008 · Cited by 134
Dynamic cross-talk between microglia and peripheral monocytes underlies stress-induced neuroinflammation and behavioral consequences
Wohleb, E. S., & Delpech, J.-C. (2016) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2016.04.013 · Cited by 132
Self-citation
Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring
Gur, T. L., Palkar, A. V., Rajasekera, T., Allen, J., Niraula, A., Godbout, J., & Bailey, M. T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.025 · Cited by 127
Microglia: A Central Player in Depression
Deng, S.-L., Chen, J.-G., & Wang, F. (2020) · Current Medical Science · doi:10.1007/s11596-020-2193-1 · Cited by 119
Inflammatory Mediators in Mood Disorders: Therapeutic Opportunities
Pfau, M. L., Ménard, C., & Russo, S. J. (2017) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010617-052823 · Cited by 118
TNFα and IL-1β but not IL-18 Suppresses Hippocampal Long-Term Potentiation Directly at the Synapse
Prieto, G. A., Tong, L., Smith, E. D., & Cotman, C. W. (2018) · Neurochemical Research · doi:10.1007/s11064-018-2517-8 · Cited by 121
Stress-Induced Microglia Activation and Monocyte Trafficking to the Brain Underlie the Development of Anxiety and Depression
Ramírez, K., Trías, J. F., & Sheridan, J. F. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_25 · Cited by 113
Self-citation
Modeling consequences of prolonged strong unpredictable stress in zebrafish: Complex effects on behavior and physiology
Song, C., Liu, B.-P., Zhang, Y., Peng, Z., Wang, J., Collier, A. D., Echevarria, D. J., Savelieva, K. V., Lawrence, R. F., Rex, C. S., et al. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.08.021 · Cited by 119
The Influence of Microglial Elimination and Repopulation on Stress Sensitization Induced by Repeated Social Defeat
Weber, M. D., McKim, D. B., Niraula, A., Witcher, K. G., Yin, W., Sobol, C. G., Wang, Y., Sawicki, C. M., Sheridan, J. F., & Godbout, J. P. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.10.009 · Cited by 112
Self-citation
Social isolation alters behavior, the gut-immune-brain axis, and neurochemical circuits in male and female prairie voles
Donovan, M., Mackey, C. S., Platt, G. N., Rounds, J., Brown, A. N., Trickey, D. J., Liu, Y., Jones, K. M., & Wang, Z. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100278 · Cited by 85
Social defeat models in animal science: What we have learned from rodent models
Toyoda, A. (2017) · Animal Science Journal · doi:10.1111/asj.12809 · Cited by 108
Electro-Acupuncture Alleviates Chronic Unpredictable Stress-Induced Depressive- and Anxiety-Like Behavior and Hippocampal Neuroinflammation in Rat Model of Depression
Yue, N., Li, B., Yang, L., Han, Q.-Q., Huang, H.-J., Wang, Y.-L., Wang, J., Yu, R., Wu, G.-C., Liu, Q., et al. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00149 · Cited by 100
Developmental microglial priming in postmortem autism spectrum disorder temporal cortex
Lee, A. S., Azmitia, E. C., & Whitaker‐Azmitia, P. M. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.01.019 · Cited by 100
Interleukin-1 receptor on hippocampal neurons drives social withdrawal and cognitive deficits after chronic social stress
DiSabato, D. J., Nemeth, D. P., Liu, X., Witcher, K. G., O’Neil, S. M., Oliver, B., Bray, C. E., Sheridan, J. F., Godbout, J. P., & Quan, N. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-0788-3 · Cited by 93
Self-citation
The emerging tale of microglia in psychiatric disorders
Rahimian, R., Wakid, M., O’Leary, L. A., & Mechawar, N. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.09.023 · Cited by 96
Cytokine alterations and cognitive impairment in major depressive disorder: From putative mechanisms to novel treatment targets
Misiak, B., Beszłej, J. A., Kotowicz, K., Szewczuk-Bogusławska, M., Samochowiec, J., Kucharska–Mazur, J., & Frydecka, D. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.04.021 · Cited by 87
Inflammation in the pathogenesis of depression: a disorder of neuroimmune origin
Corrigan, M., O’Rourke, A. M., Moran, B., Fletcher, J. M., & Harkin, A. (2023) · Neuronal Signaling · doi:10.1042/ns20220054 · Cited by 81
Sleep deprivation induces spatial memory impairment by altered hippocampus neuroinflammatory responses and glial cells activation in rats
Wadhwa, M., Kumari, P., Chauhan, G., Roy, K., Alam, S., Kishore, K., Ray, K., & Panjwani, U. (2017) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2017.09.003 · Cited by 78
Sulforaphane-Enriched Broccoli Sprouts Pretreated by Pulsed Electric Fields Reduces Neuroinflammation and Ameliorates Scopolamine-Induced Amnesia in Mouse Brain through Its Antioxidant Ability via Nrf2-HO-1 Activation
Subedi, L., Cho, K., Park, Y. U., Choi, H.-J., & Kim, S. Y. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/3549274 · Cited by 79
Chronic Cortical Inflammation, Cognitive Impairment, and Immune Reactivity Associated with Diffuse Brain Injury Are Ameliorated by Forced Turnover of Microglia
Bray, C. E., Witcher, K. G., Adekunle-Adegbite, D., Ouviña, M., Witzel, M., Hans, E., Tapp, Z. M., Packer, J. M., Goodman, E. J., Zhao, F., et al. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1910-21.2022 · Cited by 77
Self-citation
Microglia Promote Increased Pain Behavior through Enhanced Inflammation in the Spinal Cord during Repeated Social Defeat Stress
Sawicki, C. M., Kim, J. K., Weber, M. D., Faw, T. D., McKim, D. B., Madalena, K. M., Lerch, J. K., Basso, D. M., Humeidan, M., Godbout, J. P., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2785-18.2018 · Cited by 76
Self-citation
Microglial Inflammatory-Metabolic Pathways and Their Potential Therapeutic Implication in Major Depressive Disorder
Rahimian, R., Belliveau, C., Chen, R., & Mechawar, N. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.871997 · Cited by 77
Beyond the neuron: Role of non-neuronal cells in stress disorders
Cathomas, F., Holt, L. M., Parise, E. M., Liu, J., Murrough, J. W., Casaccia, P., Nestler, E. J., & Russo, S. J. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.033 · Cited by 72
Social status and modern‐type depression: A review
Komori, T., Makinodan, M., & Kishimoto, T. (2019) · Brain and Behavior · doi:10.1002/brb3.1464 · Cited by 75
Microglia and HPA axis in depression: An overview of participation and relationship
Pereira, G. C., Piton, E., dos Santos, B. M., Ramanzini, L. G., Camargo, L. F. M., da Silva, R. M., & Bochi, G. V. (2021) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2021.1939154 · Cited by 72
Stress-Related Dysfunction of Adult Hippocampal Neurogenesis—An Attempt for Understanding Resilience?
Leschik, J., Lutz, B., & Gentile, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147339 · Cited by 77
Neuroinflammatory and cognitive consequences of combined radiation and immunotherapy in a novel preclinical model
McGinnis, G. J., Friedman, D. J., Young, K. H., Torres, E. R. S., Thomas, C. R., Gough, M. J., & Raber, J. (2016) · Oncotarget · doi:10.18632/oncotarget.13551 · Cited by 75
Repeated social defeat in female mice induces anxiety-like behavior associated with enhanced myelopoiesis and increased monocyte accumulation in the brain
Yin, W., Gallagher, N. R., Sawicki, C. M., McKim, D. B., Godbout, J. P., & Sheridan, J. F. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.01.015 · Cited by 68
Self-citation
Social instability is an effective chronic stress paradigm for both male and female mice
Yohn, C. N., Ashamalla, S. A., Bokka, L., Gergues, M. M., Garino, A., & Samuels, B. A. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107780 · Cited by 71
Stress primes microglial polarization after global ischemia: Therapeutic potential of progesterone
Espinosa‐García, C., Sayeed, I., Yousuf, S., Atif, F., Sergeeva, E. G., Neigh, G. N., & Stein, D. G. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.06.012 · Cited by 65
Toll‐like receptor 2 activation and up‐regulation by high mobility group box‐1 contribute to post‐operative neuroinflammation and cognitive dysfunction in mice
Lin, F., Shan, W., Zheng, Y., Pan, L., & Zuo, Z. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15368 · Cited by 64
Ganoderic acid A exerted antidepressant-like action through FXR modulated NLRP3 inflammasome and synaptic activity
Bao, H., Li, H., Jia, Y., Xiao, Y., Luo, S., Zhang, D., Han, L., Dai, L., Xiao, C., Feng, L., et al. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114561 · Cited by 63
Role of infiltrating monocytes/macrophages in acute and chronic neuroinflammation: Effects on cognition, learning and affective behaviour
Minogue, A. M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.02.008 · Cited by 62
Tolerance-inducing effect and properties of innate immune stimulation on chronic stress-induced behavioral abnormalities in mice
Gu, Y., Ye, T., Tan, P., Tong, L., Jian-lin, J., Gu, Y., Shen, Z., Shen, X., Lu, X., & Huang, C. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.11.002 · Cited by 60
Repeated psychosocial stress causes glutamic acid decarboxylase isoform-67, oxidative-Nox-2 changes and neuroinflammation in mice: Prevention by treatment with a neuroactive flavonoid, morin
Ben‐Azu, B., Emokpae, O., Ajayi, A. M., Jarikre, T. A., Orhode, V., Aderibigbe, A. O., Umukoro, S., & Iwalewa, E. O. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146917 · Cited by 57
How stress physically re-shapes the brain: Impact on brain cell shapes, numbers and connections in psychiatric disorders
Kaul, D., Schwab, S. G., Mechawar, N., & Matosin, N. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.01.025 · Cited by 58
Neuroinflammation Regulates Cognitive Impairment in Socially Defeated Mice
Pfau, M. L., & Russo, S. J. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.04.004 · Cited by 54
Disruptive physiology: olfaction and the microbiome–gut–brain axis
Bienenstock, J., Kunze, W., & Forsythe, P. (2017) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12348 · Cited by 53
Chronic Stress Contributes to Osteosarcopenic Adiposity via Inflammation and Immune Modulation: The Case for More Precise Nutritional Investigation
Ilich, J. Z., Gilman, J. C., Cvijetić, S., & Boschiero, D. (2020) · Nutrients · doi:10.3390/nu12040989 · Cited by 51
Naringin Confers Protection against Psychosocial Defeat Stress-Induced Neurobehavioral Deficits in Mice: Involvement of Glutamic Acid Decarboxylase Isoform-67, Oxido-Nitrergic Stress, and Neuroinflammatory Mechanisms
Oladapo, O. M., Ben‐Azu, B., Ajayi, A. M., Emokpae, O., Eneni, A.-E. O., Omogbiya, I. A., & Iwalewa, E. O. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-020-01664-y · Cited by 51
The neural circuits and molecular mechanisms underlying fear dysregulation in posttraumatic stress disorder
Iqbal, J., Huang, G.-D., Xue, Y.-X., Yang, M., & Jia, X. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1281401 · Cited by 58
The Immunomodulatory Effects of Plant Extracts and Plant Secondary Metabolites on Chronic Neuroinflammation and Cognitive Aging: A Mechanistic and Empirical Review
Kure, C., Timmer, J. K., & Stough, C. K. K. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00117 · Cited by 51
The formative role of microglia in stress-induced synaptic deficits and associated behavioral consequences
Bollinger, J. L., & Wohleb, E. S. (2019) · Neuroscience Letters · doi:10.1016/j.neulet.2019.134369 · Cited by 51
Self-citation
Resveratrol ameliorates maternal separation-induced anxiety- and depression-like behaviors and reduces Sirt1-NF-kB signaling-mediated neuroinflammation
Wei, R., Zhang, Y., Feng, Y.-Z., Zhang, K.-X., Zhang, J., Chen, J., Luo, B., Li, X., & Chen, G.-H. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1172091 · Cited by 49
Implicating neuroinflammation in hippocampus, prefrontal cortex and amygdala with cognitive deficit: a narrative review
Blossom, V., Ullal, S. D., D’Souza, M. M., Ranade, A. V., Kumar, N. A., & Rai, R. (2025) · 3 Biotech · doi:10.1007/s13205-025-04468-2 · Cited by 57
Microglia under psychosocial stressors along the aging trajectory: Consequences on neuronal circuits, behavior, and brain diseases
Tian, L., Hui, C. W., Bisht, K., Tan, Y., Sharma, K. P., Chen, S., Zhang, X., & Tremblay, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.01.007 · Cited by 52
Modulation of Neural Networks by Interleukin-1
Nemeth, D. P., & Quan, N. (2020) · Brain Plasticity · doi:10.3233/bpl-200109 · Cited by 46
Neurogenic hypothesis of positive psychology in stress-induced depression: Adult hippocampal neurogenesis, neuroinflammation, and stress resilience
Wu, Z., Xiao, L., Wang, H., & Wang, G. (2021) · International Immunopharmacology · doi:10.1016/j.intimp.2021.107653 · Cited by 48
The antidepressant impact of minocycline in rodents: A systematic review and meta-analysis
Reis, D. J., Casteen, E. J., & Ilardi, S. S. (2019) · Scientific Reports · doi:10.1038/s41598-018-36507-9 · Cited by 45
Mesenchymal Stromal Cells Modulate Peripheral Stress-Induced Innate Immune Activation Indirectly Limiting the Emergence of Neuroinflammation-Driven Depressive and Anxiety-like Behaviors
Gallagher, D., Siddiqui, F., Fish, J., Charlat, M., Chaudry, E., Moolla, S., Gauthier-Fisher, A., & Librach, C. L. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.07.015 · Cited by 44
Exercise mitigates a gut microbiota-mediated reduction in adult hippocampal neurogenesis and associated behaviours in rats
Nicolas, S., Dohm-Hansen, S., Lavelle, A., Bastiaanssen, T. F. S., English, J. A., Cryan, J. F., & Nolan, Y. M. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02904-0 · Cited by 52
Normalization of HPA Axis, Cholinergic Neurotransmission, and Inhibiting Brain Oxidative and Inflammatory Dynamics Are Associated with The Adaptogenic-like Effect of Rutin Against Psychosocial Defeat Stress
Emudainohwo, J. O. T., Ben‐Azu, B., Adebayo, O. G., Aduema, W., Uruaka, C. I., Ajayi, A. M., Okpakpor, E. E., & Ozolua, R. I. (2022) · Journal of Molecular Neuroscience · doi:10.1007/s12031-022-02084-w · Cited by 46
Antidepressant‐like effects of 20(S)‐protopanaxadiol in a mouse model of chronic social defeat stress and the related mechanisms
Jiang, N., Lv, J., Wang, H., Wang, Q., Lü, C., Yang, Y., Huang, H. M., Xia, T., Lv, G., & Liu, X. (2019) · Phytotherapy Research · doi:10.1002/ptr.6446 · Cited by 42
An emerging role for microglia in stress‐effects on memory
Sanguino‐Gómez, J., Buurstede, J. C., Abiega, O., Fitzsimons, C. P., Lucassen, P. J., Eggen, B. J. L., Lesuis, S. L., Meijer, O. C., & Krugers, H. J. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15188 · Cited by 43
Social stress during adolescence activates long-term microglia inflammation insult in reward processing nuclei
Rodríguez‐Arias, M., Montagud‐Romero, S., Carrión, A. M. G., Perez, C. F., Pérez‐Villalba, A., Marco, E. M., López‐Gallardo, M., Viveros, M., & Miñarro, J. (2018) · PLoS ONE · doi:10.1371/journal.pone.0206421 · Cited by 42
Multidimensional cognitive impairment in unipolar and bipolar depression and the moderator effect of adverse childhood experiences
Poletti, S., Aggio, V., Brioschi, S., Dallaspezia, S., Colombo, C., & Benedetti, F. (2016) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12497 · Cited by 42
Anti-inflammatory agents for smoking cessation? Focus on cognitive deficits associated with nicotine withdrawal in male mice
Saravia, R., Ten-Blanco, M., Grande, M. T., Maldonado, R. J., & Berrendero, F. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.11.003 · Cited by 39
Preventive putative mechanisms involved in the psychopathologies of mice passively coping with psychosocial defeat stress by quercetin
Ugwu, P. I., Ben‐Azu, B., Ugwu, S. U., Uruaka, C. I., Nworgu, C. C., Okorie, P. O., Okafor, K. O., Anachuna, K. K., Elendu, M. U., Ugwu, A. O., et al. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.03.004 · Cited by 40
Anxious behavior induces elevated hippocampal Cb2 receptor gene expression
Robertson, J. M., Achua, J. K., Smith, J. P., Prince, M. A., Staton, C. D., Ronan, P. J., Summers, T. R., & Summers, C. H. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.03.061 · Cited by 36
Pharmacological and chemogenetic orexin/hypocretin intervention ameliorates Hipp-dependent memory impairment in the A53T mice model of Parkinson’s disease
Stanojlović, M., Pallais, J. P., Lee, M. K., & Kotz, C. M. (2019) · Molecular Brain · doi:10.1186/s13041-019-0514-8 · Cited by 35
(Putative) sex differences in neuroimmune modulation of memory
Tronson, N. C., & Collette, K. M. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23921 · Cited by 36
Microglial Dysregulation and Suicidality: A Stress-Diathesis Perspective
Baharikhoob, P., & Kolla, N. J. (2020) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2020.00781 · Cited by 40
CD36 deficiency affects depressive-like behaviors possibly by modifying gut microbiota and the inflammasome pathway in mice
Bai, S., Wang, W., Ting, W., Li, J., Zhang, S., Chen, Z., Qi, X., Chen, J., Cheng, K., & Xie, P. (2021) · Translational Psychiatry · doi:10.1038/s41398-020-01130-8 · Cited by 33
Tumor necrosis factor α negatively regulates the retrieval and reconsolidation of hippocampus-dependent memory
Takahashi, S., Fukushima, H., Yu, Z., Tomita, H., & Kida, S. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.02.033 · Cited by 33
Cannabinoid receptor 1 signalling modulates stress susceptibility and microglial responses to chronic social defeat stress
Beins, E. C., Beiert, T., Jenniches, I., Hansen, J. N., Leidmaa, E., SCHRICKEL, J. W., & Zimmer, A. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01283-0 · Cited by 33
Identification of hyper‐ramified microglia in the CA1 region of the mouse hippocampus potentially associated with stress resilience
Fujikawa, R., & Jinno, S. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15812 · Cited by 29
How stress mediators can cumulatively contribute to Alzheimer’s disease An allostatic load approach
Matos, T. M., & Souza‐Talarico, J. N. (2019) · Dementia & Neuropsychologia · doi:10.1590/1980-57642018dn13-010002 · Cited by 35
The role of physical trauma in social stress-induced immune activation
Foertsch, S., & Reber, S. O. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.025 · Cited by 31
Apoptosis-induced decline in hippocampal microglia mediates the development of depression-like behaviors in adult mice triggered by unpredictable stress during adolescence
Zhu, H., Pan, H., Fang, Y., Wang, H., Chen, Z., Hu, W., Tong, L., Ren, J., Lu, X., & Huang, C. (2024) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2024.176763 · Cited by 29
Neuroimmune Mechanisms and Sex/Gender-Dependent Effects in the Pathophysiology of Mental Disorders
Kokkosis, A. G., & Tsirka, S. E. (2020) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.120.266163 · Cited by 29
Do changes in microglial status underlie neurogenesis impairments and depressive-like behaviours induced by psychological stress? A systematic review in animal models
Nieto-Quero, A., Chaves-Peña, P., Santín, L. J., Pérez‐Martín, M., & Pedraza, C. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100356 · Cited by 32
Minocycline in Major Depressive Disorder: And overview with considerations on treatment-resistance and comparisons with other psychiatric disorders
Nettis, M. A. (2021) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2021.100335 · Cited by 32
Unique brain endothelial profiles activated by social stress promote cell adhesion, prostaglandin E2 signaling, hypothalamic–pituitary–adrenal axis modulation, and anxiety
Yin, W., Swanson, S. P., Biltz, R. G., Goodman, E. J., Gallagher, N. R., Sheridan, J. F., & Godbout, J. P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01434-x · Cited by 30
Self-citation
Localization of brain neuronal IL-1R1 reveals specific neural circuitries responsive to immune signaling
Nemeth, D. P., Liu, X., Monet, M. C., Niu, H., Maxey, G., Schrier, M. S., Smirnova, M. I., McGovern, S., Herd, A., DiSabato, D. J., et al. (2024) · Journal of Neuroinflammation · doi:10.1186/s12974-024-03287-1 · Cited by 26
Self-citation
Social experiences switch states of memory engrams through regulating hippocampal Rac1 activity
Lei, B., Lv, L., Hu, S., Tang, Y., & Zhong, Y. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2116844119 · Cited by 32
Modulation of high fat diet-induced microbiome changes, but not behaviour, by minocycline
Hasebe, K., Rivera, L. R., Smith, C. M., Allnutt, T. R., Crowley, T. M., Nelson, T. M., Dean, O. M., McGee, S. L., Walder, K. R., & Gray, L. J. (2019) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2019.09.001 · Cited by 26
The psychological consequences of (perceived) ionizing radiation exposure: a review on its role in radiation-induced cognitive dysfunction
Collett, G., Craenen, K., Young, W. R., Gilhooly, M., & Anderson, R. M. (2020) · International Journal of Radiation Biology · doi:10.1080/09553002.2020.1793017 · Cited by 32
Stress-Induced Sensitization of Angiotensin II Hypertension Is Reversed by Blockade of Angiotensin-Converting Enzyme or Tumor Necrosis Factor-α
Xue, B., Yu, Y., Wei, S., Beltz, T. G., Guo, F., Felder, R. B., & Johnson, A. K. (2019) · American Journal of Hypertension · doi:10.1093/ajh/hpz075 · Cited by 25
High-mobility group box 1-mediated hippocampal microglial activation induces cognitive impairment in mice with neuropathic pain
Hisaoka‐Nakashima, K., Ohata, K., Yoshimoto, N., Tokuda, S., Yoshii, N., Nakamura, Y., Wang, D., Liu, K., Wake, H., Yoshida, T., et al. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114146 · Cited by 26
Repeated social defeat induces transient glial activation and brain hypometabolism: A positron emission tomography imaging study
Feltes, P. K., de Vries, E. F. J., Juárez‐Orozco, L. E., Kurtys, E., Dierckx, R., Jeckel, C. M. M., & Doorduin, J. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17747189 · Cited by 24
Treatment with lysophosphatidic acid prevents microglial activation and depression-like behaviours in a murine model of neuropsychiatric systemic lupus erythematosus
Nagata, W., Koizumi, A., Nakagawa, K., Takahashi, S., Gotoh, M., Satoh, Y., & Ishizuka, T. (2023) · Clinical & Experimental Immunology · doi:10.1093/cei/uxad010 · Cited by 24
Environmental conditions differentially affect neurobehavioral outcomes in a mouse model of sepsis-associated encephalopathy
Ji, M., Tang, H. J., Luo, D., Qiu, L.-L., Jia, M., Yuan, H., Feng, S., & Yang, J. (2017) · Oncotarget · doi:10.18632/oncotarget.19595 · Cited by 23
The effects of living in an outdoor enclosure on hippocampal plasticity and anxiety‐like behavior in response to nematode infection
Cope, E. C., Opendak, M. M., LaMarca, E. A., Murthy, S. S., Park, C. Y., Olson, L. B., Martinez, S., Leung, J. M., Graham, A. L., & Gould, E. (2018) · Hippocampus · doi:10.1002/hipo.23033 · Cited by 27
Infiltrating peripheral monocyte TREM-1 mediates dopaminergic neuron injury in substantia nigra of Parkinson’s disease model mice
Song, W., Zhou, Z.-M., Zhang, L., Shu, H.-F., Xia, J.-R., Qin, X., Hua, R., & Zhang, Y. (2025) · Cell Death and Disease · doi:10.1038/s41419-025-07333-5 · Cited by 25
The Brain-Gut Axis Contributes to Neuroprogression in Stress-Related Disorders
Rea, K., Dinan, T. G., & Cryan, J. F. (2017) · Modern trends in psychiatry · doi:10.1159/000470813 · Cited by 22

Authors: McKim, D. B., Niraula, A., Tarr, A. J., Wohleb, E. S., Sheridan, J. F., & Godbout, J. P.
Affiliations: The Ohio State University Wexner Medical Center (US)
ORCID: McKim, Daniel B.
Niraula, Anzela
Wohleb, Eric S.
Sheridan, John F.
Godbout, Jonathan P.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2016-03-02
Volume: 36
Issue: 9
Pages: 2590-2604
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.2394-15.2016
PMC: PMC4879207
OpenAlex: W2292907345
Cited by: 204
References: 56
Citations by year: 2026: 6 · 2025: 16 · 2024: 18 · 2023: 15 · 2022: 24 · 2021: 21 · 2020: 24 · 2019: 21 · 2018: 20 · 2017: 24 · 2016: 12
FWCI: 14.06
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 184 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (R01AG033028)
National Institute of Mental Health (R01MH097243, F31MH109234, R01MH093473, R01-MH-093472)
National Institute of Dental and Craniofacial Research (T32DE014320)
Topics: Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: repeated social defeat, neuroinflammation, psychosocial stress, hippocampus, microglial activation, monocyte trafficking, adult neurogenesis, spatial memory impairment, social avoidance, depression-like behavior, minocycline, neuroimmune interactions, neuronal differentiation, neural progenitor cells
MeSH terms: Doublecortin Domain Proteins, Animals, Brain, Bromodeoxyuridine, Calcium-Binding Proteins, Disease Models, Animal, Encephalitis, Hippocampus, Male, Memory Disorders, Mice, Inbred C57BL, Microfilament Proteins, Microtubule-Associated Proteins, Minocycline, Neuronal Plasticity, Neuropeptides, Social Behavior, Stress, Psychological, Leukocyte Common Antigens, Maze Learning, Cell Proliferation, Mice, Neural Stem Cells

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

Neuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks