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Brain resting-state connectivity in the development of secondary hyperalgesia in healthy men

  • Morten Sejer HansenEmail author
  • Lino Becerra
  • Jørgen Berg Dahl
  • David Borsook
  • Johan Mårtensson
  • Anders Christensen
  • Janus Damm Nybing
  • Inger Havsteen
  • Mikael Boesen
  • Mohammad Sohail Asghar
Original Article
  • 34 Downloads

Abstract

Central sensitization is a condition in which there is an abnormal responsiveness to nociceptive stimuli. As such, the process may contribute to the development and maintenance of pain. Factors influencing the propensity for development of central sensitization have been a subject of intense debate and remain elusive. Injury-induced secondary hyperalgesia can be elicited by experimental pain models in humans, and is believed to be a result of central sensitization. Secondary hyperalgesia may thus reflect the individual level of central sensitization. The objective of this study was to investigate possible associations between increasing size of secondary hyperalgesia area and brain connectivity in known resting-state networks. We recruited 121 healthy participants (male, age 22, SD 3.35) who underwent resting-state functional magnetic resonance imaging. Prior to the scan session, areas of secondary hyperalgesia following brief thermal sensitization (3 min. 45 °C heat stimulation) were evaluated in all participants. 115 participants were included in the final analysis. We found a positive correlation (increasing connectivity) with increasing area of secondary hyperalgesia in the sensorimotor- and default mode networks. We also observed a negative correlation (decreasing connectivity) with increasing secondary hyperalgesia area in the sensorimotor-, fronto-parietal-, and default mode networks. Our findings indicate that increasing area of secondary hyperalgesia is associated with increasing and decreasing connectivity in multiple networks, suggesting that differences in the propensity for central sensitization, assessed as secondary hyperalgesia areas, may be expressed as differences in the resting-state central neuronal activity.

Keywords

Pain Secondary hyperalgesia Central sensitization Resting-state fMRI MRI 

Notes

Acknowledgements

We wish to thank the staff of the Department of Radiology, Bispebjerg and Frederiksberg Hospitals for support in obtaining the MRI scans.

Author contributions

All authors contributed in the conception and design of the study, and critically revised the manuscript. All authors read and approved the final manuscript.

Funding

This work is supported by grants from the Augustinus foundation (Grant number: 14-3907), Toyota Fonden—Denmark (Grant number: OH/BG-8610), the Aase and Ejnar Danielsen’s foundation (Grant number: 10-001341), and the DASAIM pain research award. Dr. Borsook received funding from NIH Grant NINDS K24 NS064050. The funders had no role in the conception or design of the study, or on the decision to publish the results.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Supplementary material

429_2018_1819_MOESM1_ESM.docx (12 kb)
Supplementary material 1 (DOCX 12 KB)
429_2018_1819_MOESM2_ESM.docx (15 kb)
Supplementary material 2 (DOCX 14 KB)

References

  1. Abou-Elseoud A, Starck T, Remes J, Nikkinen J, Tervonen O, Kiviniemi V (2010) The effect of model order selection in group PICA. Hum Brain Mapp 31(8):1207–1216.  https://doi.org/10.1002/hbm.20929 CrossRefPubMedGoogle Scholar
  2. Albert K, Pruessner J, Newhouse P (2015) Estradiol levels modulate brain activity and negative responses to psychosocial stress across the menstrual cycle. Psychoneuroendocrinology 59:14–24.  https://doi.org/10.1016/j.psyneuen.2015.04.022 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen EA, Erhardt EB, Damaraju E, Gruner W, Segall JM, Silva RF, Havlicek M, Rachakonda S, Fries J, Kalyanam R, Michael AM, Caprihan A, Turner JA, Eichele T, Adelsheim S, Bryan AD, Bustillo J, Clark VP, Feldstein Ewing SW, Filbey F, Ford CC, Hutchison K, Jung RE, Kiehl KA, Kodituwakku P, Komesu YM, Mayer AR, Pearlson GD, Phillips JP, Sadek JR, Stevens M, Teuscher U, Thoma RJ, Calhoun VD (2011) A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 5:2.  https://doi.org/10.3389/fnsys.2011.00002 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Arelin K, Mueller K, Barth C, Rekkas PV, Kratzsch J, Burmann I, Villringer A, Sacher J (2015) Progesterone mediates brain functional connectivity changes during the menstrual cycle—a pilot resting state MRI study. Front Neurosci 9:44.  https://doi.org/10.3389/fnins.2015.00044 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Asghar MS, Pereira MP, Werner MU, Martensson J, Larsson HB, Dahl JB (2015) Secondary hyperalgesia phenotypes exhibit differences in brain activation during noxious stimulation. PLoS One 10(1):e0114840.  https://doi.org/10.1371/journal.pone.0114840 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Atlas LY, Wager TD (2012) How expectations shape pain. Neurosci Lett 520(2):140–148.  https://doi.org/10.1016/j.neulet.2012.03.039 CrossRefPubMedGoogle Scholar
  7. Baliki MN, Geha PY, Apkarian AV, Chialvo DR (2008) Beyond feeling: chronic pain hurts the brain, disrupting the default-mode network dynamics. J Neurosci 28(6):1398–1403.  https://doi.org/10.1523/JNEUROSCI.4123-07.2008 CrossRefPubMedGoogle Scholar
  8. Baliki MN, Mansour AR, Baria AT, Apkarian AV (2014) Functional reorganization of the default mode network across chronic pain conditions. PLoS One 9(9):e106133.  https://doi.org/10.1371/journal.pone.0106133 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Beckmann CF, Mackay CE, Filippini N, Smith SM (2009) Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. OHBM. https://fsl.fmrib.ox.ac.uk/fsl/fslwiki/DualRegression
  10. Besag J (1986) On the statistical analysis of dirty pictures. J R Stat Soc B 48(3):259–302.  https://doi.org/10.1080/02664769300000059 CrossRefGoogle Scholar
  11. Borsook D, Upadhyay J, Chudler EH, Becerra L (2010) A key role of the basal ganglia in pain and analgesia-insights gained through human functional imaging. Mol Pain 6:27.  https://doi.org/10.1186/1744-8069-6-27 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bressler SL, Menon V (2010) Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 14(6):277–290.  https://doi.org/10.1016/j.tics.2010.04.004 CrossRefPubMedGoogle Scholar
  13. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 1124:1–38.  https://doi.org/10.1196/annals.1440.011 CrossRefPubMedGoogle Scholar
  14. Campbell CM, Edwards RR, Fillingim RB (2005) Ethnic differences in responses to multiple experimental pain stimuli. Pain 113(1–2):20–26.  https://doi.org/10.1016/j.pain.2004.08.013 CrossRefPubMedGoogle Scholar
  15. Cavallone LF, Frey K, Montana MC, Joyal J, Regina KJ, Petersen KL, Gereau RWt (2013) Reproducibility of the heat/capsaicin skin sensitization model in healthy volunteers. J Pain Res 6:771–784.  https://doi.org/10.2147/JPR.S53437 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chen S, Ross TJ, Zhan W, Myers CS, Chuang KS, Heishman SJ, Stein EA, Yang Y (2008a) Group independent component analysis reveals consistent resting-state networks across multiple sessions. Brain Res 1239:141–151.  https://doi.org/10.1016/j.brainres.2008.08.028 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chen TL, Babiloni C, Ferretti A, Perrucci MG, Romani GL, Rossini PM, Tartaro A, Del Gratta C (2008b) Human secondary somatosensory cortex is involved in the processing of somatosensory rare stimuli: an fMRI study. Neuroimage 40(4):1765–1771.  https://doi.org/10.1016/j.neuroimage.2008.01.020 CrossRefPubMedGoogle Scholar
  18. Cheng JC, Erpelding N, Kucyi A, DeSouza DD, Davis KD (2015) Individual differences in temporal summation of pain reflect pronociceptive and antinociceptive brain structure and function. J Neurosci 35(26):9689–9700.  https://doi.org/10.1523/jneurosci.5039-14.2015 CrossRefPubMedGoogle Scholar
  19. Choi JC, Park SK, Kim YH, Shin YW, Kwon JS, Kim JS, Kim JW, Kim SY, Lee SG, Lee MS (2006) Different brain activation patterns to pain and pain-related unpleasantness during the menstrual cycle. Anesthesiology 105(1):120–127CrossRefPubMedGoogle Scholar
  20. Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS (2013) Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16(9):1348–1355.  https://doi.org/10.1038/nn.3470 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103(37):13848–13853.  https://doi.org/10.1073/pnas.0601417103 CrossRefPubMedGoogle Scholar
  22. De Kock M, Lavand’homme P, Waterloos H (2001) ‘Balanced analgesia’ in the perioperative period: is there a place for ketamine? Pain 92(3):373–380CrossRefPubMedGoogle Scholar
  23. De Kock M, Lavand’homme P, Waterloos H (2005) The short-lasting analgesia and long-term antihyperalgesic effect of intrathecal clonidine in patients undergoing colonic surgery. Anesth Analg 101(2):566–572.  https://doi.org/10.1213/01.ANE.0000157121.71808.04 CrossRefPubMedGoogle Scholar
  24. Dirks J, Petersen KL, Rowbotham MC, Dahl JB (2001) Effect of systemic adenosine on pain and secondary hyperalgesia associated with the heat/capsaicin sensitization model in healthy volunteers. Reg Anesth Pain Med 26(5):414–419.  https://doi.org/10.1053/rapm.2001.22256a CrossRefPubMedGoogle Scholar
  25. Dirks J, Petersen KL, Rowbotham MC, Dahl JB (2002) Gabapentin suppresses cutaneous hyperalgesia following heat-capsaicin sensitization. Anesthesiology 97(1):102–107CrossRefPubMedGoogle Scholar
  26. Dirks J, Petersen KL, Dahl JB (2003) The heat/capsaicin sensitization model: a methodologic study. J Pain 4(3):122–128CrossRefPubMedGoogle Scholar
  27. Edwards CL, Fillingim RB, Keefe F (2001) Race, ethnicity and pain. Pain 94(2):133–137CrossRefPubMedGoogle Scholar
  28. Engman J, Linnman C, Van Dijk KR, Milad MR (2016) Amygdala subnuclei resting-state functional connectivity sex and estrogen differences. Psychoneuroendocrinology 63:34–42.  https://doi.org/10.1016/j.psyneuen.2015.09.012 CrossRefPubMedGoogle Scholar
  29. Fabian LA, McGuire L, Goodin BR, Edwards RR (2011) Ethnicity, catastrophizing, and qualities of the pain experience. Pain Med 12(2):314–321.  https://doi.org/10.1111/j.1526-4637.2010.01015.x CrossRefPubMedGoogle Scholar
  30. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci USA 106(17):7209–7214.  https://doi.org/10.1073/pnas.0811879106 CrossRefPubMedGoogle Scholar
  31. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711.  https://doi.org/10.1038/nrn2201 CrossRefPubMedGoogle Scholar
  32. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102(27):9673–9678.  https://doi.org/10.1073/pnas.0504136102 CrossRefPubMedGoogle Scholar
  33. Friedman L, Glover GH (2006) Report on a multicenter fMRI quality assurance protocol. J Magn Reson Imaging 23(6):827–839.  https://doi.org/10.1002/jmri.20583 CrossRefPubMedGoogle Scholar
  34. Frymoyer AR, Rowbotham MC, Petersen KL (2007) Placebo-controlled comparison of a morphine/dextromethorphan combination with morphine on experimental pain and hyperalgesia in healthy volunteers. J Pain 8(1):19–25.  https://doi.org/10.1016/j.jpain.2006.05.010 CrossRefPubMedGoogle Scholar
  35. Galli G, Santarnecchi E, Feurra M, Bonifazi M, Rossi S, Paulus MP, Rossi A (2016) Individual and sex-related differences in pain and relief responsiveness are associated with differences in resting-state functional networks in healthy volunteers. Eur J Neurosci 43(4):486–493.  https://doi.org/10.1111/ejn.13125 CrossRefPubMedGoogle Scholar
  36. Gear R, Becerra L, Upadhyay J, Bishop J, Wallin D, Pendse G, Levine J, Borsook D (2013) Pain facilitation brain regions activated by nalbuphine are revealed by pharmacological fMRI. PLoS One 8(1):e50169.  https://doi.org/10.1371/journal.pone.0050169 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gong G, He Y, Evans AC (2011) Brain connectivity: gender makes a difference. Neuroscientist 17(5):575–591.  https://doi.org/10.1177/1073858410386492 CrossRefPubMedGoogle Scholar
  38. Griffanti L, Salimi-Khorshidi G, Beckmann CF, Auerbach EJ, Douaud G, Sexton CE, Zsoldos E, Ebmeier KP, Filippini N, Mackay CE, Moeller S, Xu J, Yacoub E, Baselli G, Ugurbil K, Miller KL, Smith SM (2014) ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging. Neuroimage 95:232–247.  https://doi.org/10.1016/j.neuroimage.2014.03.034 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Guo CC, Kurth F, Zhou J, Mayer EA, Eickhoff SB, Kramer JH, Seeley WW (2012) One-year test–retest reliability of intrinsic connectivity network fMRI in older adults. Neuroimage 61(4):1471–1483.  https://doi.org/10.1016/j.neuroimage.2012.03.027 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Han S, Ma Y (2014) Cultural differences in human brain activity: a quantitative meta-analysis. Neuroimage 99:293–300.  https://doi.org/10.1016/j.neuroimage.2014.05.062 CrossRefPubMedGoogle Scholar
  41. Hansen MS, Asghar MS, Wetterslev J, Pipper CB, Johan Martensson J, Becerra L, Christensen A, Nybing JD, Havsteen I, Boesen M, Dahl JB (2016a) Is the volume of the caudate nuclei associated with area of secondary hyperalgesia? Protocol for a 3-tesla MRI study of healthy volunteers. JMIR Res Protoc 5(2):e117.  https://doi.org/10.2196/resprot.5680 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hansen MS, Wetterslev J, Pipper CB, Asghar MS, Dahl JB (2016b) Is heat pain detection threshold associated with the area of secondary hyperalgesia following brief thermal sensitization? A study of healthy volunteers—design and detailed plan of analysis. BMC Anesthesiol 16(1):28.  https://doi.org/10.1186/s12871-016-0193-2 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hansen MS, Wetterslev J, Pipper CB, Ostervig R, Asghar MS, Dahl JB (2016c) The area of secondary hyperalgesia following heat stimulation in healthy male volunteers: inter- and intra-individual variance and reproducibility. PLoS One 11(5):e0155284.  https://doi.org/10.1371/journal.pone.0155284 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hansen MS, Wetterslev J, Pipper CB, Asghar MS, Dahl JB (2017) Heat pain detection threshold is associated with the area of secondary hyperalgesia following brief thermal sensitization: a study of healthy male volunteers. J Pain Res 10:265–274.  https://doi.org/10.2147/JPR.S121189 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Hansen MS, Asghar MS, Wetterslev J, Pipper CB, Martensson J, Becerra L et al (2018) The association between areas of secondary hyperalgesia and volumes of the caudate nuclei and other pain relevant brain structures-A 3-tesla MRI study of healthy men. PLoS One 13(8):e0201642CrossRefPubMedPubMedCentralGoogle Scholar
  46. Hjelmervik H, Hausmann M, Osnes B, Westerhausen R, Specht K (2014) Resting states are resting traits—an FMRI study of sex differences and menstrual cycle effects in resting state cognitive control networks. PLoS One 9(7):e103492CrossRefPubMedPubMedCentralGoogle Scholar
  47. Iacovides S, Avidon I, Baker FC (2015) Does pain vary across the menstrual cycle? A review. Eur J Pain 19(10):1389–1405.  https://doi.org/10.1002/ejp.1714 (Epub 2015 Apr 1321) CrossRefPubMedGoogle Scholar
  48. Jensen MT, Petersen KL (2006) Gender differences in pain and secondary hyperalgesia after heat/capsaicin sensitization in healthy volunteers. J Pain 7(3):211–217.  https://doi.org/10.1016/j.jpain.2005.10.013 CrossRefPubMedGoogle Scholar
  49. Kong J, Jensen K, Loiotile R, Cheetham A, Wey HY, Tan Y, Rosen B, Smoller JW, Kaptchuk TJ, Gollub RL (2013) Functional connectivity of the frontoparietal network predicts cognitive modulation of pain. Pain 154(3):459–467.  https://doi.org/10.1016/j.pain.2012.12.004 CrossRefPubMedGoogle Scholar
  50. Kregel J, Meeus M, Malfliet A, Dolphens M, Danneels L, Nijs J, Cagnie B (2015) Structural and functional brain abnormalities in chronic low back pain: a systematic review. Semin Arthritis Rheum 45(2):229–237.  https://doi.org/10.1016/j.semarthrit.2015.05.002 CrossRefPubMedGoogle Scholar
  51. Kringelbach ML, Rolls ET (2004) The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 72(5):341–372.  https://doi.org/10.1016/j.pneurobio.2004.03.006 CrossRefPubMedGoogle Scholar
  52. Latremoliere A, Woolf CJ (2009) Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 10(9):895–926.  https://doi.org/10.1016/j.jpain.2009.06.012 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lee MC, Zambreanu L, Menon DK, Tracey I (2008) Identifying brain activity specifically related to the maintenance and perceptual consequence of central sensitization in humans. J Neurosci 28(45):11642–11649.  https://doi.org/10.1523/jneurosci.2638-08.2008 CrossRefPubMedGoogle Scholar
  54. Lorenz J, Minoshima S, Casey KL (2003) Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. Brain 126(Pt 5):1079–1091CrossRefPubMedGoogle Scholar
  55. Lu S, Gao W, Wei Z, Wang D, Hu S, Huang M, Xu Y, Li L (2016) Intrinsic brain abnormalities in young healthy adults with childhood trauma: a resting-state functional magnetic resonance imaging study of regional homogeneity and functional connectivity. Aust N Z J Psychiatry.  https://doi.org/10.1177/0004867416671415 CrossRefPubMedGoogle Scholar
  56. Marsaglia G, Tsang W, Wang J (2003) Evaluating Kolmogorov’s distribution. J Stat Softw 8(18):1–4CrossRefGoogle Scholar
  57. Martinez V, Ben Ammar S, Judet T, Bouhassira D, Chauvin M, Fletcher D (2012) Risk factors predictive of chronic postsurgical neuropathic pain: the value of the iliac crest bone harvest model. Pain 153(7):1478–1483.  https://doi.org/10.1016/j.pain.2012.04.004 CrossRefPubMedGoogle Scholar
  58. Massey FJ (1951) The Kolmogorov–Smirnov test for goodness of fit. J Am Stat Assoc 46(253):68–78CrossRefGoogle Scholar
  59. Mikkelsen S, Dirks J, Fabricius P, Petersen KL, Rowbotham MC, Dahl JB (2001) Effect of intravenous magnesium on pain and secondary hyperalgesia associated with the heat/capsaicin sensitization model in healthy volunteers. Br J Anaesth 86(6):871–873CrossRefPubMedGoogle Scholar
  60. Mohan A, Roberto AJ, Mohan A, Lorenzo A, Jones K, Carney MJ, Liogier-Weyback L, Hwang S, Lapidus KA (2016) The significance of the default mode network (DMN) in neurological and neuropsychiatric disorders: a review. Yale J Biol Med 89(1):49–57PubMedPubMedCentralGoogle Scholar
  61. Moiniche S, Dahl JB, Kehlet H (1993) Time course of primary and secondary hyperalgesia after heat injury to the skin. Br J Anaesth 71(2):201–205CrossRefPubMedGoogle Scholar
  62. Morris VH, Cruwys SC, Kidd BL (1997) Characterisation of capsaicin-induced mechanical hyperalgesia as a marker for altered nociceptive processing in patients with rheumatoid arthritis. Pain 71(2):179–186CrossRefPubMedGoogle Scholar
  63. Morris V, Cruwys S, Kidd B (1998) Increased capsaicin-induced secondary hyperalgesia as a marker of abnormal sensory activity in patients with fibromyalgia. Neurosci Lett 250(3):205–207CrossRefPubMedGoogle Scholar
  64. Mosteller RD (1987) Simplified calculation of body-surface area. N Engl J Med 317(17):1098.  https://doi.org/10.1056/NEJM198710223171717 CrossRefPubMedGoogle Scholar
  65. Nichols T, Hayasaka S (2003) Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res 12(5):419–446CrossRefPubMedGoogle Scholar
  66. Noonan MP, Kolling N, Walton ME, Rushworth MF (2012) Re-evaluating the role of the orbitofrontal cortex in reward and reinforcement. Eur J Neurosci 35(7):997–1010.  https://doi.org/10.1111/j.1460-9568.2012.08023.x CrossRefPubMedGoogle Scholar
  67. Ostergard T, Munyon C, Miller JP (2014) Motor cortex stimulation for chronic pain. Neurosurg Clin N Am 25(4):693–698.  https://doi.org/10.1016/j.nec.2014.06.004 CrossRefPubMedGoogle Scholar
  68. Palermo S, Benedetti F, Costa T, Amanzio M (2015) Pain anticipation: an activation likelihood estimation meta-analysis of brain imaging studies. Hum Brain Mapp 36(5):1648–1661.  https://doi.org/10.1002/hbm.22727 CrossRefPubMedGoogle Scholar
  69. Pedersen JL, Kehlet H (1998) Secondary hyperalgesia to heat stimuli after burn injury in man. Pain 76(3):377–384CrossRefPubMedGoogle Scholar
  70. Pendse G, Borsook D, Becerra L (2009) Enhanced false discovery rate using Gaussian mixture models for thresholding fMRI statistical maps. Neuroimage 47(1):231–261.  https://doi.org/10.1016/j.neuroimage.2009.02.035 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Petersen N, Cahill L (2015) Amygdala reactivity to negative stimuli is influenced by oral contraceptive use. Soc Cogn Affect Neurosci 10(9):1266–1272.  https://doi.org/10.1093/scan/nsv1010. (Epub 2015 Feb 1216) CrossRefPubMedPubMedCentralGoogle Scholar
  72. Petersen KL, Rowbotham MC (1999) A new human experimental pain model: the heat/capsaicin sensitization model. Neuroreport 10(7):1511–1516CrossRefPubMedGoogle Scholar
  73. Petersen KL, Brennum J, Dahl JB (1997) Experimental evaluation of the analgesic effect of ibuprofen on primary and secondary hyperalgesia. Pain 70(2–3):167–174CrossRefPubMedGoogle Scholar
  74. Petersen KL, Jones B, Segredo V, Dahl JB, Rowbotham MC (2001) Effect of remifentanil on pain and secondary hyperalgesia associated with the heat–capsaicin sensitization model in healthy volunteers. Anesthesiology 94(1):15–20CrossRefPubMedGoogle Scholar
  75. Petersen KL, Meadoff T, Press S, Peters MM, LeComte MD, Rowbotham MC (2008) Changes in morphine analgesia and side effects during daily subcutaneous administration in healthy volunteers. Pain 137(2):395–404.  https://doi.org/10.1016/j.pain.2007.09.019 CrossRefPubMedGoogle Scholar
  76. Petersen KL, Iyengar S, Chappell AS, Lobo ED, Reda H, Prucka WR, Verfaille SJ (2014) Safety, tolerability, pharmacokinetics, and effects on human experimental pain of the selective ionotropic glutamate receptor 5 (iGluR5) antagonist LY545694 in healthy volunteers. Pain 155(5):929–936.  https://doi.org/10.1016/j.pain.2014.01.019 CrossRefPubMedGoogle Scholar
  77. Peyron R, Schneider F, Faillenot I, Convers P, Barral FG, Garcia-Larrea L, Laurent B (2004) An fMRI study of cortical representation of mechanical allodynia in patients with neuropathic pain. Neurology 63(10):1838–1846CrossRefPubMedGoogle Scholar
  78. Peyron R, Faillenot I, Mertens P, Laurent B, Garcia-Larrea L (2007) Motor cortex stimulation in neuropathic pain. Correlations between analgesic effect and hemodynamic changes in the brain. A PET study. Neuroimage 34(1):310–321.  https://doi.org/10.1016/j.neuroimage.2006.08.037 CrossRefPubMedGoogle Scholar
  79. Rahim-Williams B, Riley JL 3rd, Williams AK, Fillingim RB (2012) A quantitative review of ethnic group differences in experimental pain response: do biology, psychology, and culture matter? Pain Med 13(4):522–540.  https://doi.org/10.1111/j.1526-4637.2012.01336.x CrossRefPubMedPubMedCentralGoogle Scholar
  80. Raichle ME (2015) The brain’s default mode network. Annu Rev Neurosci 38:433–447.  https://doi.org/10.1146/annurev-neuro-071013-014030 CrossRefPubMedGoogle Scholar
  81. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98(2):676–682.  https://doi.org/10.1073/pnas.98.2.676 CrossRefPubMedGoogle Scholar
  82. Richmond S, Johnson KA, Seal ML, Allen NB, Whittle S (2016) Development of brain networks and relevance of environmental and genetic factors: a systematic review. Neurosci Biobehav Rev 71:215–239.  https://doi.org/10.1016/j.neubiorev.2016.08.024 CrossRefPubMedGoogle Scholar
  83. Sala-Llonch R, Bartres-Faz D, Junque C (2015) Reorganization of brain networks in aging: a review of functional connectivity studies. Front Psychol 6:663.  https://doi.org/10.3389/fpsyg.2015.00663 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Salengros JC, Huybrechts I, Ducart A, Faraoni D, Marsala C, Barvais L, Cappello M, Engelman E (2010) Different anesthetic techniques associated with different incidences of chronic post-thoracotomy pain: low-dose remifentanil plus presurgical epidural analgesia is preferable to high-dose remifentanil with postsurgical epidural analgesia. J Cardiothorac Vasc Anesth 24(4):608–616.  https://doi.org/10.1053/j.jvca.2009.10.006 CrossRefPubMedGoogle Scholar
  85. Salimi-Khorshidi G, Douaud G, Beckmann CF, Glasser MF, Griffanti L, Smith SM (2014) Automatic denoising of functional MRI data: combining independent component analysis and hierarchical fusion of classifiers. Neuroimage 90:449–468.  https://doi.org/10.1016/j.neuroimage.2013.11.046 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27(9):2349–2356.  https://doi.org/10.1523/JNEUROSCI.5587-06.2007 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Seifert F, Bschorer K, De Col R, Filitz J, Peltz E, Koppert W, Maihofner C (2009) Medial prefrontal cortex activity is predictive for hyperalgesia and pharmacological antihyperalgesia. J Neurosci 29(19):6167–6175.  https://doi.org/10.1523/JNEUROSCI.4654-6108.2009 CrossRefPubMedGoogle Scholar
  88. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17(3):143–155.  https://doi.org/10.1002/hbm.10062 CrossRefPubMedGoogle Scholar
  89. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci USA 106(31):13040–13045.  https://doi.org/10.1073/pnas.0905267106 CrossRefPubMedGoogle Scholar
  90. Smith SM, Miller KL, Moeller S, Xu J, Auerbach EJ, Woolrich MW, Beckmann CF, Jenkinson M, Andersson J, Glasser MF, Van Essen DC, Feinberg DA, Yacoub ES, Ugurbil K (2012) Temporally-independent functional modes of spontaneous brain activity. Proc Natl Acad Sci USA 109(8):3131–3136.  https://doi.org/10.1073/pnas.1121329109 CrossRefPubMedGoogle Scholar
  91. Stein N, Sprenger C, Scholz J, Wiech K, Bingel U (2012) White matter integrity of the descending pain modulatory system is associated with interindividual differences in placebo analgesia. Pain 153(11):2210–2217.  https://doi.org/10.1016/j.pain.2012.07.010 CrossRefPubMedGoogle Scholar
  92. Tanji J, Hoshi E (2008) Role of the lateral prefrontal cortex in executive behavioral control. Physiol Rev 88(1):37–57.  https://doi.org/10.1152/physrev.00014.2007 CrossRefPubMedGoogle Scholar
  93. Timmermann L, Ploner M, Haucke K, Schmitz F, Baltissen R, Schnitzler A (2001) Differential coding of pain intensity in the human primary and secondary somatosensory cortex. J Neurophysiol 86(3):1499–1503CrossRefPubMedGoogle Scholar
  94. Tracey I (2007) Neuroimaging of pain mechanisms. Curr Opin Support Palliat Care 1(2):109–116.  https://doi.org/10.1097/SPC.0b013e3282efc58b CrossRefPubMedGoogle Scholar
  95. Tracey I (2008) Imaging pain. Br J Anaesth 101(1):32–39.  https://doi.org/10.1093/bja/aen102 CrossRefPubMedGoogle Scholar
  96. Tracey I, Mantyh PW (2007) The cerebral signature for pain perception and its modulation. Neuron 55(3):377–391.  https://doi.org/10.1016/j.neuron.2007.07.012 CrossRefPubMedGoogle Scholar
  97. van den Heuvel MP, Hulshoff Pol HE (2010) Exploring the brain network: a review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20(8):519–534.  https://doi.org/10.1016/j.euroneuro.2010.03.008 CrossRefPubMedGoogle Scholar
  98. Veldhuijzen DS, Greenspan JD, Kim JH, Coghill RC, Treede RD, Ohara S, Lenz FA (2007) Imaging central pain syndromes. Curr Pain Headache Rep 11(3):183–189CrossRefPubMedGoogle Scholar
  99. Vierck CJ, Whitsel BL, Favorov OV, Brown AW, Tommerdahl M (2013) Role of primary somatosensory cortex in the coding of pain. Pain 154(3):334–344.  https://doi.org/10.1016/j.pain.2012.10.021 CrossRefPubMedGoogle Scholar
  100. Vincent K, Tracey I (2010) Sex hormones and pain: the evidence from functional imaging. Curr Pain Headache Rep 14(5):396–403.  https://doi.org/10.1007/s11916-11010-10139-11911 CrossRefPubMedGoogle Scholar
  101. Vogt BA (2016) Midcingulate cortex: Structure, connections, homologies, functions and diseases. J Chem Neuroanat 74:28–46.  https://doi.org/10.1016/j.jchemneu.2016.01.010 CrossRefPubMedGoogle Scholar
  102. Wager TD (2005) The Neural bases of placebo effects in pain. Curr Dir Psychol Sci 14(4):175–179.  https://doi.org/10.1111/j.0963-7214.2005.00359.x CrossRefGoogle Scholar
  103. Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL, Davidson RJ, Kosslyn SM, Rose RM, Cohen JD (2004) Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 303(5661):1162–1167.  https://doi.org/10.1126/science.1093065 CrossRefPubMedGoogle Scholar
  104. Wager TD, Scott DJ, Zubieta JK (2007) Placebo effects on human mu-opioid activity during pain. Proc Natl Acad Sci USA 104(26):11056–11061.  https://doi.org/10.1073/pnas.0702413104 CrossRefPubMedGoogle Scholar
  105. Werner MU, Petersen KL, Rowbotham MC, Dahl JB (2013) Healthy volunteers can be phenotyped using cutaneous sensitization pain models. PLoS One 8(5):e62733  https://doi.org/10.61371/journal.pone.0062733.Print0062013 CrossRefPubMedPubMedCentralGoogle Scholar
  106. Wisner KM, Atluri G, Lim KO, Macdonald AW 3rd (2013) Neurometrics of intrinsic connectivity networks at rest using fMRI: retest reliability and cross-validation using a meta-level method. Neuroimage 76:236–251.  https://doi.org/10.1016/j.neuroimage.2013.02.066 CrossRefPubMedGoogle Scholar
  107. Woolf CJ (2011) Central sensitization: implications for the diagnosis and treatment of pain. Pain 152 (3 Suppl):S2–S15.  https://doi.org/10.1016/j.pain.2010.1009.1030 (Epub 2010 Oct 1018) CrossRefPubMedGoogle Scholar
  108. Woolrich MW, Behrens TE, Beckmann CF, Smith SM (2005) Mixture models with adaptive spatial regularization for segmentation with an application to FMRI data. IEEE Trans Med Imaging 24(1):1–11CrossRefPubMedGoogle Scholar
  109. Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12(6):900–918.  https://doi.org/10.1038/jcbfm.1992.127 CrossRefPubMedGoogle Scholar
  110. Yelnik J (2008) Modeling the organization of the basal ganglia. Rev Neurol (Paris) 164(12):969–976.  https://doi.org/10.1016/j.neurol.2008.04.019 CrossRefGoogle Scholar
  111. Zhang J, Su J, Wang M, Zhao Y, Yao Q, Zhang Q, Lu H, Zhang H, Wang S, Li GF, Wu YL, Liu FD, Shi YH, Li J, Liu JR, Du X (2016) Increased default mode network connectivity and increased regional homogeneity in migraineurs without aura. J Headache Pain 17(1):98.  https://doi.org/10.1186/s10194-016-0692-z CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Morten Sejer Hansen
    • 1
    • 2
    Email author return OK on get
  • Lino Becerra
    • 3
  • Jørgen Berg Dahl
    • 4
  • David Borsook
    • 5
    • 6
    • 7
  • Johan Mårtensson
    • 8
  • Anders Christensen
    • 2
  • Janus Damm Nybing
    • 2
  • Inger Havsteen
    • 2
  • Mikael Boesen
    • 9
  • Mohammad Sohail Asghar
    • 10
  1. 1.Department of Anaesthesiology, 4231, Centre of Head and OrthopaedicsRigshospitaletCopenhagenDenmark
  2. 2.Department of RadiologyCopenhagen University Hospital Bispebjerg and FrederiksbergCopenhagenDenmark
  3. 3.Invicro, A Konica Minolta CompanyBostonUSA
  4. 4.Department of AnaesthesiologyCopenhagen University Hospital Bispebjerg and FrederiksbergCopenhagenDenmark
  5. 5.Department of Radiology, Athinoula A. Martinos Center for Biomedical ImagingMassachusetts General HospitalCharlestownUSA
  6. 6.Department of Psychiatry, McLean HospitalHarvard Medical SchoolBostonUSA
  7. 7.Department of Psychiatry, Massachusetts General HospitalHarvard Medical SchoolBostonUSA
  8. 8.Department of Clinical Sciences, Faculty of MedicineLund UniversityLundSweden
  9. 9.Department of Radiology and the Parker InstituteCopenhagen University Hospital Bispebjerg and Frederiksberg, Bispebjerg HospitalCopenhagenDenmark
  10. 10.Department of Neuroanaesthesiology, NeurocentreRigshospitaletCopenhagenDenmark

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