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Chronic Pain Impairs Memory Formation via Disruption of Neurogenesis Mediated by Mesohippocampal Brain-Derived Neurotrophic Factor Signaling

  • Author Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
    Sun-Hui Xia
    Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Author Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
    Su-Wan Hu
    Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
    Search for articles by this author
  • Author Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
    De-Gao Ge
    Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Di Liu
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Di Wang
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Song Zhang
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Qi Zhang
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Ling Yuan
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Yan-Qiang Li
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Jun-Xia Yang
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Peng Wu
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Hongxing Zhang
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Ming-Hu Han
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Department of Pharmacological Sciences, Institute for Systems Biomedicine, Icahn School of Medicine at Mount Sinai, New York, New York

    Fishberg Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, New York
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  • Hai-Lei Ding
    Correspondence
    Hai-Lei Ding, Ph.D.
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China
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  • Jun-Li Cao
    Correspondence
    Address correspondence to Jun-Li Cao, M.D. Ph.D.
    Affiliations
    Jiangsu Province Key Laboratory of Anesthesiology, Xuzhou Medical University, Xuzhou, China

    Jiangsu Province Key Laboratory of Anesthesia and Analgesia Application Technology, Xuzhou Medical University, Xuzhou, China

    Department of Anesthesiology, Affiliated Hospital of Xuzhou Medical University, Xuzhou, China
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  • Author Footnotes
    1 S-HX, S-WH, and D-GG contributed equally to this work.
Published:February 21, 2020DOI:https://doi.org/10.1016/j.biopsych.2020.02.013

      Abstract

      Background

      Chronic pain patients often complain of their poor memory. The mechanisms underlying chronic pain–related memory impairment remain elusive, and there are few clinical therapeutic strategies available for this condition.

      Methods

      In a neuropathic pain model induced by chronic constrictive injury of the sciatic nerve in male mice, we used circuit-specific electrophysiological recording, combined with chemogenetic, molecular, and pharmacologic methods, to examine the circuit and molecular mechanisms underlying chronic pain–related memory impairment.

      Results

      Our current results show that chronic neuropathic pain impaired the acquisition of spatial memory and, meanwhile, reduced adult neurogenesis in the dentate gyrus. Experimentally reducing dentate gyrus neurogenesis mimicked this pain-induced effect on spatial memory formation in naïve mice. Furthermore, pain-associated impairments of both hippocampal neurogenesis and memory formation were rescued or mimicked by chemogenetic activation or deactivation, respectively, of the ventral tegmental area dopaminergic projection, through which ventral tegmental area–released brain-derived neurotrophic factor was required. Importantly, we found that chronic, but not acute, systematic administration of subanesthetic doses of ketamine, while without relieving pain, ameliorated chronic pain–related impairment of spatial memory formation, potentially by rescuing brain-derived neurotrophic factor–mediated dentate gyrus neurogenesis.

      Conclusions

      These findings provide a novel, circuit-based mechanistic link between chronic pain and memory formation deficit, and potential new therapeutic options for chronic pain–related learning deficit and memory impairment.

      Keywords

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      Linked Article

      • The Many Avenues Leading to Adult Neurogenesis Adaptations
        Biological PsychiatryVol. 88Issue 8
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          Adult hippocampal neurogenesis (AHN) is a phenomenon by which the brain responds to biological and environmental clues by producing new neurons in selected brain regions of adult mammals, including humans (1,2). There has been an ongoing debate regarding the presence of AHN in humans and about the role that adult-born neurons might have in cognition and behavior (3). Functions related to AHN are dependent not just on neurogenesis per se, but on the ability of newborn neurons to survive, differentiate, and integrate in the dentate gyrus (DG) circuit.
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