Neuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat

McKim, Daniel B.; Niraula, Anzela; Tarr, Andrew J.; Wohleb, Eric S.; Sheridan, John F.; Godbout, Jonathan P.

doi:10.1523/jneurosci.2394-15.2016

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

Neuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat

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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

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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.

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Inhibiting microglia during stress exposure with minocycline attenuated the increase of proinflammatory cytokines normally produced by stress and protected against stress-associated deficits in cognitive memory tasks and depressive-like and anxiety-like behaviors.
“In each case, inhibiting microglia during stress exposure attenuated the increase of proinflammatory cytokines normally produced by stress (Hinwood et al, 2012(Hinwood et al, , 2013;;Kreisel et al, 2014;McKim et al, 2016).”
From Repeated Social Defeat, Neuroinflammation, and Behavior: Monocytes Carry the Signal (2017) · cites this paper as McKim et al, 2016
Increased corticosterone has also been associated with the impaired hippocampal neurogenesis and neuronal development in the context of psychological stress.
“Increased corticosterone has also been associated with the impaired hippocampal neurogenesis and neuronal development in the context of psychological stress (Lehmann et al, 2013;McKim et al, 2016).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as McKim et al, 2016

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Repeated social defeat stress induces neuroinflammation and impairs hippocampal neurogenesis that differentially regulate mood and cognition
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Neuroinflammation Regulates Cognitive Impairment in Socially Defeated Mice
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Blood-borne factors regulate monocyte function during psychosocial stress: A case of corticosterone and IL6
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Self-citation

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

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Neuroinflammatory Dynamics Underlie Memory Impairments after Repeated Social Defeat

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