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Influence of Cerebral Glucose Metabolism by Chronic Pain–Mediated Cognitive Impairment in Adolescent Rats

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Abstract

Chronic pain during adolescence can lead to mental health disorders in adulthood, but the underlying mechanism is still unclear. Furthermore, the homeostasis of cerebral glucose metabolism and neurotransmitter metabolic kinetics are closely associated with cognitive development and pain progression. The present study investigated changes in cognitive function and glucose metabolism in adult rats, which had experienced chronic pain during their adolescence. Here, spared nerve injury (SNI) surgery was conducted in 4-week-old male rats. Mechanical nociceptive reflex thresholds were analyzed, and SNI chronic pain (SNI-CP) animals were screened. Based on animal behavioral tests (open field, three-chambered social, novel object recognition and the Y maze), the SNI-CP animals showed learning and memory impairment and anxiety-like behaviors, compared to SNI no chronic pain (SNI-NCP) animals. The cerebral glucose metabolism in the prefrontal cortex and hippocampus of adult SNI-CP animals was decreased with positron emission tomography/computed tomography. GABA2 and Glu4 levels in the metabolic kinetics study were significantly decreased in the hippocampus, frontal cortex, and temporal cortex, and the expression of GLUT3 and GLUT4 was also significantly downregulated in the prefrontal cortex and hippocampus of adult rats in the SNI-CP group. These findings suggest that the rats which suffered chronic pain during adolescence have lower cerebral glucose metabolism in the cortex and hippocampus, which could be related to cognitive function during the development of the central nervous system.

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Availability of Data and Materials

All raw data and materials during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

We wish to thank Yingying Chen, Department of Anaesthesiology, Zhongnan Hospital, Wuhan University, for her help in cartoon illustrating.

Funding

This work was supported by the National Natural Science Foundation of China (NO. 81771160, 31771193 and 81901109).

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  1. Yuanyuan Fang and Chang Chen contributed equally to this work.

Authors and Affiliations

  1. Department of Anaesthesiology, Zhongnan Hospital, Wuhan University, Wuhan, Hubei, 430071, People’s Republic of China

    Yuanyuan Fang, Chang Chen, Qi Zhong, Lirong Wang, Jinpiao Zhu & Zongze Zhang

  2. Key Laboratory of Magnetic Resonance in Biological Systems, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, National Center for Magnetic Resonance in Wuhan, Wuhan Institute of Physics and Mathematics, Innovation Academy for Precision Measurement Science and Technology, Chinese Academy of Sciences-Wuhan National Laboratory for Optoelectronics, Wuhan, Hubei, 430071, People’s Republic of China

    Zhu Gui, Jinpiao Zhu, Fuqiang Xu & Jie Wang

  3. School of Human and Social Sciences, University of West London, Brentford, TW8 9GA, Middlesex, UK

    Anne Manyande

  4. Institute of Neuroscience and Brain Diseases, Xiangyang Central Hospital, Affiliated Hospital of Hubei University of Arts and Science, Xiangyang, Hubei, People’s Republic of China

    Jie Wang

  5. University of Chinese Academy of Sciences, Beijing, 100049, People’s Republic of China

    Jie Wang

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Yuanyuan Fang, Chang Chen, Jie Wang, and Zongze Zhang designed the study; Yuanyuan Fang, Qi Zhong, Lirong Wang, Zhu Gui, and Jinpiao Zhu performed the experiments; Yuanyuan Fang, Chang Chen, Jie Wang, and Fuqiang Xu contributed to the data. Yuanyuan Fang, Chang Chen, Jie Wang, Zongze Zhang, and Anne Manyande wrote the manuscript. The content of this manuscript has been reviewed, read, and agreed upon by all the designated authors.

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Fang, Y., Chen, C., Zhong, Q. et al. Influence of Cerebral Glucose Metabolism by Chronic Pain–Mediated Cognitive Impairment in Adolescent Rats. Mol Neurobiol 59, 3635–3648 (2022). https://doi.org/10.1007/s12035-022-02816-4

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