Skip to main content

Advertisement

SpringerLink
Log in

Preoperative Acute Sleep Deprivation Causes Postoperative Pain Hypersensitivity and Abnormal Cerebral Function

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

Preoperative sleep loss can amplify post-operative mechanical hyperalgesia. However, the underlying mechanisms are still largely unknown. In the current study, rats were randomly allocated to a control group and an acute sleep deprivation (ASD) group which experienced 6 h ASD before surgery. Then the variations in cerebral function and activity were investigated with multi-modal techniques, such as nuclear magnetic resonance, functional magnetic resonance imaging, c-Fos immunofluorescence, and electrophysiology. The results indicated that ASD induced hyperalgesia, and the metabolic kinetics were remarkably decreased in the striatum and midbrain. The functional connectivity (FC) between the nucleus accumbens (NAc, a subregion of the ventral striatum) and the ventrolateral periaqueductal gray (vLPAG) was significantly reduced, and the c-Fos expression in the NAc and the vLPAG was suppressed. Furthermore, the electrophysiological recordings demonstrated that both the neuronal activity in the NAc and the vLPAG, and the coherence of the NAc-vLPAG were suppressed in both resting and task states. This study showed that neuronal activity in the NAc and the vLPAG were weakened and the FC between the NAc and the vLPAG was also suppressed in rats with ASD-induced hyperalgesia. This study highlights the importance of preoperative sleep management for surgical patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Stewart NH, Arora VM. Sleep in hospitalized older adults. Sleep Med Clin 2018, 13: 127–135.

    Article  PubMed  Google Scholar 

  2. Wesselius HM, van den Ende ES, Alsma J, Ter Maaten JC, Schuit SCE, Stassen PM. Quality and quantity of sleep and factors associated with sleep disturbance in hospitalized patients. JAMA Intern Med 2018, 178: 1201–1208.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Wang PK, Cao J, Wang HZ, Liang LL, Zhang J, Lutz BM, et al. Short-term sleep disturbance-induced stress does not affect basal pain perception, but does delay postsurgical pain recovery. J Pain 2015, 16: 1186–1199.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Taylor DJ, Mallory LJ, Lichstein KL, Durrence HH, Riedel BW, Bush AJ. Comorbidity of chronic insomnia with medical problems. Sleep 2007, 30: 213–218.

    Article  PubMed  Google Scholar 

  5. Hambrecht-Wiedbusch VS, Gabel M, Liu LJ, Imperial JP, Colmenero AV, Vanini G. Preemptive caffeine administration blocks the increase in postoperative pain caused by previous sleep loss in the rat: A potential role for preoptic adenosine A2A receptors in sleep-pain interactions. Sleep 2017, https://doi.org/10.1093/sleep/zsx116.

    Article  PubMed  Google Scholar 

  6. Xue JJ, Li HL, Xu ZQ, Ma DX, Guo RJ, Yang KH, et al. Paradoxical sleep deprivation aggravates and prolongs incision-induced pain hypersensitivity via BDNF signaling-mediated descending facilitation in rats. Neurochem Res 2018, 43: 2353–2361.

    Article  CAS  PubMed  Google Scholar 

  7. Li Q, Zhu ZY, Lu J, Chao YC, Zhou XX, Huang Y, et al. Sleep deprivation of rats increases postsurgical expression and activity of L-type calcium channel in the dorsal root ganglion and slows recovery from postsurgical pain. Acta Neuropathol Commun 2019, 7: 217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Haack M, Mullington JM. Sustained sleep restriction reduces emotional and physical well-being. Pain 2005, 119: 56–64.

    Article  PubMed  Google Scholar 

  9. Roehrs T, Hyde M, Blaisdell B, Greenwald M, Roth T. Sleep loss and REM sleep loss are hyperalgesic. Sleep 2006, 29: 145–151.

    Article  PubMed  Google Scholar 

  10. Centers for Disease Control and Prevention (CDC). Short sleep duration among workers—United States, 2010. MMWR Morb Mortal Wkly Rep 2012, 61: 281–285.

  11. Vanini G. Nucleus accumbens: A novel forebrain mechanism underlying the increase in pain sensitivity caused by rapid eye movement sleep deprivation. Pain 2018, 159: 5–6.

    Article  PubMed  Google Scholar 

  12. Krause AJ, Prather AA, Wager TD, Lindquist MA, Walker MP. The pain of sleep loss: A brain characterization in humans. J Neurosci 2019, 39: 2291–2300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chee MWL, Zhou J. Functional connectivity and the sleep-deprived brain. Prog Brain Res 2019, 246: 159–176.

    Article  PubMed  Google Scholar 

  14. Marques-Carneiro JE, Nehlig A, Cassel JC, Castro-Neto EF, Litzahn JJ, Pereira de Vasconcelos A, et al. Neurochemical changes and c-fos mapping in the brain after carisbamate treatment of rats subjected to lithium-pilocarpine-induced status epilepticus. Pharmaceuticals (Basel) 2017, 10: 85.

    Article  PubMed  Google Scholar 

  15. Monosov IE, Trageser JC, Thompson KG. Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field. Neuron 2008, 57: 614–625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Li B, Gong L, Wu RQ, Li AN, Xu FQ. Complex relationship between BOLD-fMRI and electrophysiological signals in different olfactory bulb layers. Neuroimage 2014, 95: 29–38.

    Article  PubMed  Google Scholar 

  17. El Hamrani D, Gin H, Gallis JL, Bouzier-Sore AK, Beauvieux MC. Consumption of alcopops during brain maturation period: Higher impact of fructose than ethanol on brain metabolism. Front Nutr 2018, 5: 33.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Liu Q, Li AN, Gong L, Zhang L, Wu N, Xu FQ. Decreased coherence between the two olfactory bulbs in Alzheimer’s disease model mice. Neurosci Lett 2013, 545: 81–85.

    Article  CAS  PubMed  Google Scholar 

  19. Vanini G. Sleep deprivation and recovery sleep prior to a noxious inflammatory insult influence characteristics and duration of pain. Sleep 2016, 39: 133–142.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Vanini G, koNemanis K, Baghdoyan HA, Lydic R. GABAergic transmission in rat pontine reticular formation regulates the induction phase of anesthesia and modulates hyperalgesia caused by sleep deprivation. Eur J Neurosci 2014, 40: 2264–2273.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Chung S, Weber F, Zhong P, Tan CL, Nguyen TN, Beier KT, et al. Identification of preoptic sleep neurons using retrograde labelling and gene profiling. Nature 2017, 545: 477–481.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Brennan TJ, Vandermeulen EP, Gebhart GF. Characterization of a rat model of incisional pain. Pain 1996, 64: 493–502.

    Article  PubMed  Google Scholar 

  23. Song ZP, Xiong BR, Zheng H, Manyande A, Guan XH, Cao F, et al. STAT1 as a downstream mediator of ERK signaling contributes to bone cancer pain by regulating MHC II expression in spinal microglia. Brain Behav Immun 2017, 60: 161–173.

    Article  CAS  PubMed  Google Scholar 

  24. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53: 55–63.

    Article  CAS  PubMed  Google Scholar 

  25. Wang N, Zhao LC, Zheng YQ, Dong MJ, Su YC, Chen WJ, et al. Alteration of interaction between astrocytes and neurons in different stages of diabetes: A nuclear magnetic resonance study using[1-(13)C]glucose and[2-(13)C]acetate. Mol Neurobiol 2015, 51: 843–852.

    Article  CAS  PubMed  Google Scholar 

  26. Wu L, Niu ZF, Hu XL, Liu HL, Li S, Chen L, et al. Regional cerebral metabolic levels and turnover in awake rats after acute or chronic spinal cord injury. FASEB J 2020, 34: 10547–10559.

    Article  CAS  PubMed  Google Scholar 

  27. Guo MM, Fang YY, Zhu JP, Chen C, Zhang ZZ, Tian XB, et al. Investigation of metabolic kinetics in different brain regions of awake rats using the[1H-13C]-NMR technique. J Pharm Biomed Anal 2021, 204: 114240.

    Article  CAS  PubMed  Google Scholar 

  28. Wang J, Jiang L, Jiang Y, Ma X, Chowdhury GM, Mason GF. Regional metabolite levels and turnover in the awake rat brain under the influence of nicotine. J Neurochem 2010, 113: 1447–1458.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Sibson NR, Mason GF, Shen J, Cline GW, Herskovits AZ, Wall JE, et al. In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during. J Neurochem 2001, 76: 975–989.

    Article  CAS  PubMed  Google Scholar 

  30. Liu TT, Li ZQ, He JD, Yang N, Han DY, Li Y, et al. Regional metabolic patterns of abnormal postoperative behavioral performance in aged mice assessed by 1 H-NMR dynamic mapping method. Neurosci Bull 2020, 36: 25–38.

    Article  CAS  PubMed  Google Scholar 

  31. Wang J, Zeng HL, Du HY, Liu ZY, Cheng J, Liu TT, et al. Evaluation of metabolites extraction strategies for identifying different brain regions and their relationship with alcohol preference and gender difference using NMR metabolomics. Talanta 2018, 179: 369–376.

    Article  CAS  PubMed  Google Scholar 

  32. Zheng DH, Li Z, Li S, Li XH, Kamal GM, Liu CY, et al. Identification of metabolic kinetic patterns in different brain regions using metabolomics methods coupled with various discriminant approaches. J Pharm Biomed Anal 2021, 198: 114027.

    Article  CAS  PubMed  Google Scholar 

  33. Liu TT, He ZG, Tian XB, Kamal GM, Li ZX, Liu ZY, et al. Specific patterns of spinal metabolites underlying α-Me-5-HT-evoked pruritus compared with histamine and capsaicin assessed by proton nuclear magnetic resonance spectroscopy. Biochim Biophys Acta Mol Basis Dis 2017, 1863: 1222–1230.

    Article  CAS  PubMed  Google Scholar 

  34. de Graaf RA, Mason GF, Patel AB, Behar KL, Rothman DL. In vivo 1H-[13C]-NMR spectroscopy of cerebral metabolism. NMR Biomed 2003, 16: 339–357.

    Article  PubMed  Google Scholar 

  35. Chen L, Li S, Zhou Y, Liu TT, Cai AL, Zhang ZZ, et al. Neuronal mechanisms of adenosine A2A receptors in the loss of consciousness induced by propofol general anesthesia with functional magnetic resonance imaging. J Neurochem 2021, 156: 1020–1032.

    Article  CAS  PubMed  Google Scholar 

  36. Kwok CHT, Learoyd AE, Canet-Pons J, Trang T, Fitzgerald M. Spinal interleukin-6 contributes to central sensitisation and persistent pain hypersensitivity in a model of juvenile idiopathic arthritis. Brain Behav Immun 2020, 90: 145–154.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Liu Y, Cheng J, Liu HL, Deng YH, Wang J, Xu FQ. NMRSpec: An integrated software package for processing and analyzing one dimensional nuclear magnetic resonance spectra. Chemom Intell Lab Syst 2017, 162: 142–148.

    Article  CAS  Google Scholar 

  38. Barrière DA, Magalhães R, Novais A, Marques P, Selingue E, Geffroy F, et al. The SIGMA rat brain templates and atlases for multimodal MRI data analysis and visualization. Nat Commun 2019, 10: 5699.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Luo YJ, Li YD, Wang L, Yang SR, Yuan XS, Wang J, et al. Nucleus accumbens controls wakefulness by a subpopulation of neurons expressing dopamine D 1 receptors. Nat Commun 2018, 9: 1576.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Seminowicz DA, Remeniuk B, Krimmel SR, Smith MT, Barrett FS, Wulff AB, et al. Pain-related nucleus accumbens function: Modulation by reward and sleep disruption. Pain 2019, 160: 1196–1207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Wang F, Sun WJ, Chang L, Sun KF, Hou LY, Qian LN, et al. cFos-ANAB: A cFos-based web tool for exploring activated neurons and associated behaviors. Neurosci Bull 2021, 37: 1441–1453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tomim DH, Pontarolla FM, Bertolini JF, Arase M, Tobaldini G, Lima MMS, et al. The pronociceptive effect of paradoxical sleep deprivation in rats: Evidence for a role of descending pain modulation mechanisms. Mol Neurobiol 2016, 53: 1706–1717.

    Article  CAS  PubMed  Google Scholar 

  43. Rechtschaffen A, Bergmann BM, Gilliland MA, Bauer K. Effects of method, duration, and sleep stage on rebounds from sleep deprivation in the rat. Sleep 1999, 22: 11–31.

    Article  CAS  PubMed  Google Scholar 

  44. Sutton BC, Opp MR. Sleep fragmentation exacerbates mechanical hypersensitivity and alters subsequent sleep-wake behavior in a mouse model of musculoskeletal sensitization. Sleep 2014, 37: 515–524.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Tiede W, Magerl W, Baumgärtner U, Durrer B, Ehlert U, Treede RD. Sleep restriction attenuates amplitudes and attentional modulation of pain-related evoked potentials, but augments pain ratings in healthy volunteers. Pain 2010, 148: 36–42.

    Article  PubMed  Google Scholar 

  46. Briggs C, Hirasawa M, Semba K. Sleep deprivation distinctly alters glutamate transporter 1 apposition and excitatory transmission to orexin and MCH neurons. J Neurosci 2018, 38: 2505–2518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Liang ZF, King J, Zhang NY. Anticorrelated resting-state functional connectivity in awake rat brain. Neuroimage 2012, 59: 1190–1199.

    Article  PubMed  Google Scholar 

  48. Benarroch EE. Involvement of the nucleus accumbens and dopamine system in chronic pain. Neurology 2016, 87: 1720–1726.

    Article  PubMed  Google Scholar 

  49. Mitsi V, Zachariou V. Modulation of pain, nociception, and analgesia by the brain reward center. Neuroscience 2016, 338: 81–92.

    Article  CAS  PubMed  Google Scholar 

  50. Wu XB, Zhu Q, Gao YJ. CCL2/CCR2 contributes to the altered excitatory-inhibitory synaptic balance in the nucleus accumbens shell following peripheral nerve injury-induced neuropathic pain. Neurosci Bull 2021, 37: 921–933.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 2000, 84: 3072–3077.

    Article  CAS  PubMed  Google Scholar 

  52. Oishi Y, Xu Q, Wang L, Zhang BJ, Takahashi K, Takata Y, et al. Slow-wave sleep is controlled by a subset of nucleus accumbens core neurons in mice. Nat Commun 2017, 8: 734.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Sardi NF, Tobaldini G, Morais RN, Fischer L. Nucleus accumbens mediates the pronociceptive effect of sleep deprivation: The role of adenosine A2A and dopamine D2 receptors. Pain 2018, 159: 75–84.

    Article  CAS  PubMed  Google Scholar 

  54. Lin XX, Itoga CA, Taha S, Li MH, Chen R, Sami K, et al. c-Fos mapping of brain regions activated by multi-modal and electric foot shock stress. Neurobiol Stress 2018, 8: 92–102.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Sardi NF, Lazzarim MK, Guilhen VA, Marcílio RS, Natume PS, Watanabe TC, et al. Chronic sleep restriction increases pain sensitivity over time in a periaqueductal gray and nucleus accumbens dependent manner. Neuropharmacology 2018, 139: 52–60.

    Article  CAS  PubMed  Google Scholar 

  56. Bagley EE, Ingram SL. Endogenous opioid peptides in the descending pain modulatory circuit. Neuropharmacology 2020, 173: 108131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Lu J, Jhou TC, Saper CB. Identification of wake-active dopaminergic neurons in the ventral periaqueductal gray matter. J Neurosci 2006, 26: 193–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Skinner GO, Damasceno F, Gomes A, de Almeida OMMS. Increased pain perception and attenuated opioid antinociception in paradoxical sleep-deprived rats are associated with reduced tyrosine hydroxylase staining in the periaqueductal gray matter and are reversed by L-dopa. Pharmacol Biochem Behav 2011, 99: 94–99.

    Article  CAS  PubMed  Google Scholar 

  59. Srinath R, Ray S. Effect of amplitude correlations on coherence in the local field potential. J Neurophysiol 2014, 112: 741–751.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Alexandre C, Latremoliere A, Ferreira A, Miracca G, Yamamoto M, Scammell TE, et al. Decreased alertness due to sleep loss increases pain sensitivity in mice. Nat Med 2017, 23: 768–774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Zhao C, Guo L, Dong JY, Cai ZW. Mass spectrometry imaging-based multi-modal technique: Next-generation of biochemical analysis strategy. Innovation (Camb) 2021, 2: 100151.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (82071208, 81870851, 31771193, and 81971775), the Outstanding Talented Young Doctor Program of Hubei Province (HB20200407), the Translational Medicine, and interdisciplinary Research Joint Fund of Zhongnan Hospital of Wuhan University (ZNJC202012), the Medical Sci-Tech Innovation Platform of Zhongnan Hospital of Wuhan University, and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB32030200).

Author information

Author notes

  1. Meimei Guo and Yuxiang Wu contributed equally to this work.

Authors and Affiliations

  1. Department of Anesthesiology, Zhongnan Hospital of Wuhan University, Wuhan, 430071, China

    Meimei Guo, Lei Chen, Bingrui Xiong, Ke Li, Zongze Zhang & Mian Peng

  2. Department of Health and Kinesiology, School of Physical Education, Jianghan University, Wuhan, 430056, China

    Yuxiang Wu

  3. 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, 430071, China

    Danhao Zheng, Jinfeng Wu, Li Wang, Fuqiang Xu & Jie Wang

  4. Department of Anesthesiology, Peking University Third Hospital, Beijing, 100191, China

    Lei Chen

  5. Department of Affective Disorders, The Affiliated Brain Hospital of Guangzhou Medical University, Guangzhou, 510000, China

    Kangguang Lin

  6. School of Human and Social Sciences, University of West London, London, W1S 3PR, UK

    Anne Manyande

  7. Institute of Neuroscience and Brain Disease; Xiangyang Central Hospital, Affiliated Hospital of Hubei University of Arts and Science, Xiangyang, 441000, China

    Jie Wang

  8. University of Chinese Academy of Sciences, Beijing, 100049, China

    Jie Wang

Authors
  1. Meimei Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuxiang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Danhao Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bingrui Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinfeng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ke Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Li Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kangguang Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zongze Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Anne Manyande
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Fuqiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Mian Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jie Wang or Mian Peng.

Ethics declarations

Conflict of interest

The authors declare no financial or non-financial conflicts of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 94 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, M., Wu, Y., Zheng, D. et al. Preoperative Acute Sleep Deprivation Causes Postoperative Pain Hypersensitivity and Abnormal Cerebral Function. Neurosci. Bull. 38, 1491–1507 (2022). https://doi.org/10.1007/s12264-022-00955-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-022-00955-1

Keywords

Search

Navigation