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Paradoxical Sleep Deprivation Aggravates and Prolongs Incision-Induced Pain Hypersensitivity via BDNF Signaling-Mediated Descending Facilitation in Rats

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Abstract

The mechanisms underlying the pronociceptive effect of paradoxical sleep deprivation (PSD) are not fully established. The modulation of BDNF signaling-mediated descending facilitation from the rostral ventromedial medulla (RVM) of brain stem has been demonstrated in persistent pain models of inflammatory pain, but not in incisional pain model. Recent study has shown that PSD increases the expression of brain-derived neurotrophic factor (BDNF) in the brainstem structure. Therefore, in the current study, we asked whether the BDNF signaling-mediated descending facilitation was involved in the PSD-induced pronociceptive effect on incisional pain and delay the recovery period of postoperative pain in rats. Our results found that a preoperative 24 h PSD significantly aggravated the pain hypersensitivity after incision and prolonged the duration of postoperative pain. The lesions of ipsilateral dorsolateral funiculus partly reversed the PSD-induced pronociceptive effect on incisional pain. Interestingly, the 24 h PSD, but not incision significantly enhanced the levels of BDNF protein expression in the RVM areas of rats. Furthermore, at 1 day or 4 days after incision, intra-RVM microinjection of a BDNF antibody partly reversed the PSD-induced pronociceptive effects in incisional rats, while it did not change the cumulative pain scores and paw withdrawal thresholds in rats receiving only plantar incision. These findings suggest that the preoperative PSD may aggravate and prolong the incision-induced pain hypersensitivity via BDNF signaling-mediated descending facilitation.

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Funding

This work was funded by National Natural Science Foundation of China (Grant No. 81771181 and 81571065) and Natural Science Foundation of Beijing Municipality (Grant No. 7152056).

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Author notes

  1. Jianjun Xue and Huili Li have equally contributed to the work.

Authors and Affiliations

  1. Department of Anesthesiology, Chinese Traditional Medicine Hospital of Gansu Province, Lanzhou, 730050, Gansu, China

    Jianjun Xue & Ziqing Xu

  2. Evidence Based Medicine Center, School of Basic Medical Sciences, Lanzhou University, Lanzhou, 730050, Gansu, China

    Jianjun Xue & Kehu Yang

  3. Key Laboratory of Evidence Based Medicine and Knowledge Translation of Gansu Province, Lanzhou, 730050, Gansu, China

    Jianjun Xue & Kehu Yang

  4. Department of Anesthesiology, Beijing Chaoyang Hospital, Capital Medical University, No. 8, Gongtinan Road, Chaoyang District, Beijing, 100025, China

    Huili Li, Danxu Ma, Ruijuan Guo & Yun Wang

Authors
  1. Jianjun Xue
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  2. Huili Li
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  3. Ziqing Xu
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  7. Yun Wang
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Correspondence to Kehu Yang or Yun Wang.

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Xue, J., Li, H., Xu, Z. et al. Paradoxical Sleep Deprivation Aggravates and Prolongs Incision-Induced Pain Hypersensitivity via BDNF Signaling-Mediated Descending Facilitation in Rats. Neurochem Res 43, 2353–2361 (2018). https://doi.org/10.1007/s11064-018-2660-2

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  • DOI: https://doi.org/10.1007/s11064-018-2660-2

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