Development and sensory experience dependent regulation of microglia in barrel cortex

Kalambogias, John; Chen, Chia‐Chien; Khan, Safraz; Son, Titus; Wercberger, Racheli; Headlam, Carolyn; Lin, Cindy S.‐Y.; Brumberg, Joshua C.

doi:10.1002/cne.24771

Cited by 14 publications

(17 citation statements)

References 64 publications

(161 reference statements)

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“…Microglia undergo morphological changes from a resting state into altered state with retracted processes and expanded soma size during sensory deprivation via whisker deprivation. Sensory restoration from whisker regrowth reverts these altered microglia morphological changes back to age-matched control mice (Kalambogias et al, 2020), indicating that microglia may be recruited to neuronal structural remodeling in response to alteration in sensory input during developmental critical periods.…”

Section: Microglia and Experience-dependent Plasticitymentioning

confidence: 87%

“…LTP and LTD) partially via the PI3K, BDNF and CREB signaling (Chen et al, 2017;Burk et al, 2018;Raghuraman et al, 2019;Saw et al, 2020). Because microglia regulate synaptic plasticity which is the cellular mechanism of learning and memory (Lisman et al, 2018), several recent studies demonstrate the critical role of microglia in normal learning and memory, including memory strength and quality (Vainchtein et al, 2018;Wang et al, 2020), and in experience-dependent plasticity including the plasticity in the barrel cortex after the removal of whiskers and in the visual cortex after monocular deprivation (Sipe et al, 2016;Wang et al, 2016;Kalambogias et al, 2020). Due to the importance of microglia in synaptic pruning, synaptic plasticity and learning and memory, it is not surprising that abnormal microglia activation and the resulting neuroinflammation have been shown to be a main causal mechanism of the cognitive deficits associated with normal aging and different diseases including AD, TBI, HAND, and mental disorders such as autism, depression and PTSD (Fu et al, 2016;Kim et al, 2017;Ulland et al, 2017;Elmore et al, 2018;Krukowski et al, 2018;Lee et al, 2018;Zöller et al, 2018;Rawat et al, 2019;Li et al, 2020bLi et al, , 2021Makinde et al, 2020;Meilandt et al, 2020;Nguyen et al, 2020;Worthen et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…The barrel cortex is located in the rodent primary somatosensory cortex processing signals from the vibrissae. A recent study shows that microglia are involved in the modulation of neuronal structural remodeling in response to alteration in whisker sensory input (Kalambogias et al, 2020). Microglia undergo morphological changes from a resting state into altered state with retracted processes and expanded soma size during sensory deprivation via whisker deprivation.…”

Section: Microglia and Experience-dependent Plasticitymentioning

confidence: 99%

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Microglia regulation of synaptic plasticity and learning and memory

Cornell¹,

Salinas²,

Huang³

et al. 2022

Neural Regen Res

241

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Microglia are the resident macrophages of the central nervous system. Microglia possess varied morphologies and functions. Under normal physiological conditions, microglia mainly exist in a resting state and constantly monitor their microenvironment and survey neuronal and synaptic activity. Through the C1q, C3 and CR3 “Eat Me” and CD47 and SIRPα “Don’t Eat Me” complement pathways, as well as other pathways such as CX3CR1 signaling, resting microglia regulate synaptic pruning, a process crucial for the promotion of synapse formation and the regulation of neuronal activity and synaptic plasticity. By mediating synaptic pruning, resting microglia play an important role in the regulation of experience-dependent plasticity in the barrel cortex and visual cortex after whisker removal or monocular deprivation, and also in the regulation of learning and memory, including the modulation of memory strength, forgetfulness, and memory quality. As a response to brain injury, infection or neuroinflammation, microglia become activated and increase in number. Activated microglia change to an amoeboid shape, migrate to sites of inflammation and secrete proteins such as cytokines, chemokines and reactive oxygen species. These molecules released by microglia can lead to synaptic plasticity and learning and memory deficits associated with aging, Alzheimer’s disease, traumatic brain injury, HIV-associated neurocognitive disorder, and other neurological or mental disorders such as autism, depression and post-traumatic stress disorder. With a focus mainly on recently published literature, here we reviewed the studies investigating the role of resting microglia in synaptic plasticity and learning and memory, as well as how activated microglia modulate disease-related plasticity and learning and memory deficits. By summarizing the function of microglia in these processes, we aim to provide an overview of microglia regulation of synaptic plasticity and learning and memory, and to discuss the possibility of microglia manipulation as a therapeutic to ameliorate cognitive deficits associated with aging, Alzheimer’s disease, traumatic brain injury, HIV-associated neurocognitive disorder, and mental disorders.

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Section: Microglia and Experience-dependent Plasticitymentioning

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Section: Microglia and Experience-dependent Plasticitymentioning

confidence: 99%

See 1 more Smart Citation

Microglia regulation of synaptic plasticity and learning and memory

Cornell¹,

Salinas²,

Huang³

et al. 2022

Neural Regen Res

241

View full text Add to dashboard Cite

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“…Microglia become transformed to reactive state in response upon activation and polarization toward the lesion site [64]. Also, reactive microglia have been reported in the SSP of a murine model of experimental autoimmune encephalomyelitis [65], and in mice with whiskers unilaterally trimmed [66], suggesting that microglial morphological plasticity is responsive to alterations in sensory input. Initial reports documented that overexpression of MCP-1 in mice shows increased Iba-1 immunoreactivity [67].…”

Section: Discussionmentioning

confidence: 99%

MCP-1 Signaling Disrupts Social Behavior by Modulating Brain Volumetric Changes and Microglia Morphology

et al. 2021

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Autism spectrum disorder (ASD) is a disease characterized by reduced social interaction and stereotypic behaviors and related to macroscopic volumetric changes in cerebellar and somatosensory cortices (SPP). Epidemiological and preclinical models have confirmed that a proinflammatory profile during fetal development increases ASD susceptibility after birth. Here, we aimed to globally identify the effect of maternal exposure to high-energy dense diets, which we refer to as cafeteria diet (CAF) on peripheral and central proinflammatory profiles, microglia reactivity, and volumetric brain changes related to assisting defective social interaction in the mice offspring. We found a sex-dependent effect of maternal exposure to CAF diet or inoculation of the dsARN mimetic Poly (I:C) on peripheral proinflammatory and social interaction in the offspring. Notably, maternal exposure to CAF diet impairs social interaction and favors an increase in anxiety in male but not female offspring. Also, CAF diet exposure or Poly (I:C) inoculation during fetal programming promote peripheral proinflammatory profile in the ASD-diagnosed male but not in females. Selectively, we found a robust accumulation of the monocyte chemoattractant protein-1 (MCP-1) in plasma of ASD-diagnosed males exposed to CAF during fetal development. Biological assessment of MCP-1 signaling in brain confirms that systemic injection of MCP-1-neutralizing antibody reestablished social interaction and blocked anxiety, accompanied by a reduction in cerebellar lobule X (CbX) volume and an increase volume of the primary somatosensory (SSP) cortex in male offspring. These data highlight the contribution of diet-dependent MCP-1 signaling on volumetric brain changes and microglia morphology promoting ASD-like behavior in male mice.

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“…Num. ab5076, RRID: AB_2224402; Gonzalez Fleitas et al, ; Kalambogias et al, ; Matsuda et al, ; VanRyzin et al, ; S. B. Zhang et al, ) (Ito et al, ), a member of the calcium‐binding group of proteins that is specifically expressed in microglia (Imai, Ibata, Ito, Ohsawa, & Kohsaka, ). Tissue sections corresponding to the cortex, hippocampus, and striatum were co‐stained with anti‐Iba1 antibody and anti‐NCoR1 (Figures a and b) or anti‐SMRT antibodies (Figures b and b).…”

Section: Resultsmentioning

confidence: 99%

A cell type‐specific expression map of NCoR1 and SMRT transcriptional co‐repressors in the mouse brain

Iemolo

Montilla‐Perez

Lai

et al. 2020

J of Comparative Neurology

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The ability to rapidly change gene expression patterns is essential for differentiation, development, and functioning of the brain. Throughout development, or in response to environmental stimuli, gene expression patterns are tightly regulated by the dynamic interplay between transcription activators and repressors. Nuclear receptor corepressor 1 (NCoR1) and silencing mediator for retinoid or thyroid-hormone receptors (SMRT) are the best characterized transcriptional co-repressors from a molecular point of view. They mediate epigenetic silencing of gene expression in a wide range of developmental and homeostatic processes in many tissues, including the brain. For instance, NCoR1 and SMRT regulate neuronal stem cell proliferation and differentiation during brain development and they have been implicated in learning and memory. However, we still have a limited understanding of their regional and cell type-specific expression in the brain. In this study, we used fluorescent immunohistochemistry to map their expression patterns throughout the adult mouse brain. Our findings reveal that NCoR1 and SMRT share an overall neuroanatomical distribution, and are detected in both excitatory and inhibitory neurons. However, we observed striking differences in their cell type-specific expression in glial cells. Specifically, all oligodendrocytes express NCoR1, but only a subset express SMRT. In addition, NCoR1, but not SMRT, was detected in a subset of astrocytes and in the microglia. These novel observations are corroborated by single cell transcriptomics and emphasize how NCoR1 and SMRT may contribute to distinct biological functions, suggesting an exclusive role of NCoR1 in innate immune responses in the brain.

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Development and sensory experience dependent regulation of microglia in barrel cortex

Cited by 14 publications

References 64 publications

Microglia regulation of synaptic plasticity and learning and memory

Microglia regulation of synaptic plasticity and learning and memory

MCP-1 Signaling Disrupts Social Behavior by Modulating Brain Volumetric Changes and Microglia Morphology

A cell type‐specific expression map of NCoR1 and SMRT transcriptional co‐repressors in the mouse brain

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