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Individual Differences in Pain Sensitivity Vary as a Function of Precuneus Reactivity

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Abstract

Although humans differ widely in how sensitive they are to painful stimuli, the neural correlates underlying such variability remains poorly understood. A better understanding of this is important given that baseline pain sensitivity scores relate closely to the risk of developing refractory, chronic pain. To address this, we used a matched perception paradigm which allowed us to control for individual variations in subjective experience. By measuring subjective pain, nociceptive flexion reflexes, and, somatosensory evoked brain potentials (with source localization analysis), we were able to map the brain’s sequential response to pain while also investigating its relationship to pain sensitivity (i.e. change in the stimulation strength necessary to experience pain) and spinal cord activity. We found that pain sensitivity in healthy adults was closely tied to pain-evoked responses in the contralateral precuneus. Importantly, the precuneus did not contribute to the actual representation of pain in the brain, suggesting that pain sensitivity and pain representation depend on separate neuronal sub-systems.

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Notes

  1. Although we could have used a matched stimulation intensity paradigm, where stimulation strength was matched across participants and subjective experience was left free to vary, this approach was not favoured because it cannot guarantee that all (if any) participants will actually experience a transition from a non-painful to a painful state. As a result, the data would not have been interpretable specifically in terms of pain sensitivity.

  2. Although descending, supra-spinal control(s) can affect the withdrawal reflex response, it is important to keep in mind that the amplitude of the withdrawal reflex response represents the net, integrated set of influences impacting nociceptive signals at the spinal level (and also ascending from the spine to the brain). Thus, the withdrawal reflex response serves as a useful, non-invasive marker of net, integrated nociceptive activity occurring at the spinal level.

References

  • Apkarian AV, Bushnell MC, Treede RD, Zubieta JK (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9:463–484

    Article  PubMed  Google Scholar 

  • Baliki MN, Geha PY, Apkarian AV (2009) Parsing pain perception between nociceptive representation and magnitude estimation. J Neurophysiol 101:875–887

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carlsson K, Andersson J, Petrovic P, Petersson KM, Ohman A, Ingvar M (2006) Predictability modulates the affective and sensory-discriminative neural processing of pain. Neuroimage 32:1804–1814

    Article  PubMed  Google Scholar 

  • Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129:564–583

    Article  PubMed  Google Scholar 

  • Coghill RC, Mchaffie JG, Yen YF (2003) Neural correlates of interindividual differences in the subjective experience of pain. Proc Natl Acad Sci USA 100:8538–8542

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dowman R (1994) SEP topographies elicited by innocuous and noxious sural nerve stimulation. I. Identification of stable periods and individual differences. Electroencephalogr Clin Neurophysiol 92:291–302

    Article  CAS  PubMed  Google Scholar 

  • Dowman R, Darcey TM (1994) SEP topographies elicited by innocuous and noxious sural nerve stimulation. III. Dipole source localization analysis. Electroencephalogr Clin Neurophysiol 92:373–391

    Article  CAS  PubMed  Google Scholar 

  • Dowman R, Darcey T, Barkan H, Thadani V, Roberts D (2007) Human intracranially-recorded cortical responses evoked by painful electrical stimulation of the sural nerve. Neuroimage 34:743–763

    Article  CAS  PubMed  Google Scholar 

  • Duerden EG, Albanese MC (2013) Localization of pain-related brain activation: a meta-analysis of neuroimaging data. Hum Brain Mapp 34:109–149

    Article  PubMed  Google Scholar 

  • Garcia-Larrea L (2006) Chapter 30 evoked potentials in the assessment of pain. Handb Clin Neurol 81:439-4XI

    Google Scholar 

  • Garcia-Larrea L, Frot M, Valeriani M (2003) Brain generators of laser-evoked potentials: from dipoles to functional significance. Neurophysiol Clin 33:279–292

    Article  CAS  PubMed  Google Scholar 

  • Goffaux P, redmond WJ, Rainville P, Marchand S (2007) Descending analgesia: when the spine echoes what the brain expects. Pain 130:137–143

    Article  PubMed  Google Scholar 

  • Granot M (2009) Can we predict persistent postoperative pain by testing preoperative experimental pain? Curr Opin Anaesthesiology 22:425–430

    Article  PubMed  Google Scholar 

  • Hsu YW, Somma J, Hung YC, Tsai PS, Yang CH, Chen CC (2005) Predicting postoperative pain by preoperative pressure pain assessment. Anesthesiology 103:613–618

    Article  PubMed  Google Scholar 

  • Johnson MK, Raye CL, Mitchell KJ, Touryan SR, Greene EJ, Nolen-Hoeksema S (2006) Dissociating medial frontal and posterior cingulate activity during self-reflection. Soc Cogn Affect Neurosci 1:56–64

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee MC, Mouraux A, Iannetti GD (2009) Characterizing the cortical activity through which pain emerges from nociception. J Neurosci 29:7909–7916

    Article  CAS  PubMed  Google Scholar 

  • Legrain V, Iannetti GD, Plaghki L, Mouraux A (2011) The pain matrix reloaded: a salience detection system for the body. Prog Neurobiol 93:111–124

    Article  PubMed  Google Scholar 

  • Napadow V, LaCount L, Park K, As-Sanie S, Clauw DJ, Harris RE (2010) Intrinsic brain connectivity in fibromyalgia is associated with chronic pain intensity. Arthritis Rheum 62:2545–2555

    Article  PubMed Central  PubMed  Google Scholar 

  • Napadow V, Kim J, Clauw DJ, Harris RE (2012) Decreased intrinsic brain connectivity is associated with reduced clinical pain in fibromyalgia. Arthritis Rheum 64(7):2398–2403

    Article  PubMed Central  PubMed  Google Scholar 

  • Nielsen PR, Norgaard L, Rasmussen LS, Kehlet H (2007) Prediction of post-operative pain by an electrical pain stimulus. Acta Anaesthesiol Scand 51:582–586

    Article  CAS  PubMed  Google Scholar 

  • Nir RR, Lev R, Moont R, Granovsky Y, Sprecher E, Yarnitsky D (2008) Neurophysiology of the cortical pain network: revisiting the role of S1 in subjective pain perception via standardized low-resolution brain electromagnetic tomography (sLORETA). J Pain 9:1058–1069

    Article  PubMed  Google Scholar 

  • Pan PH, Coghill R, Houle TT, Seid MH, Lindel WM, Parker RL, Washburn SA, Harris L, Eisenach JC (2006) Multifactorial preoperative predictors for postcesarean section pain and analgesic requirement. Anesthesiology 104:417–425

    Article  PubMed  Google Scholar 

  • Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12

    PubMed  Google Scholar 

  • Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol 18:49–65

    Article  CAS  PubMed  Google Scholar 

  • Price DD, McGrath P, Rafii A, Buckingham B (1983) The validation of visual analogue scales as ratio scale measures for chronic and experimental pain. Pain 17:45–56

    Article  CAS  PubMed  Google Scholar 

  • Rolke R, Baron R, Maier C, Tolle TR, Treede RD, Beyer A, Binder A, Birbaumer N, Birklein F, Botefur IC (2006) Quantitative sensory testing in the German research network on neuropathic pain (DFNS): standardized protocol and reference values. Pain 123:231–243

    Article  CAS  PubMed  Google Scholar 

  • Sandrini G, Serrao M, Rossi P, Romaniello A, Cruccu G, Willer JC (2005) The lower limb flexion reflex in humans. Prog Neurobiol 77:353–395

    Article  PubMed  Google Scholar 

  • Schulz E, Tiemann L, Schuster T, Gross J, Ploner M (2011) Neurophysiological coding of traits and states in the perception of pain. Cereb Cortex 21:2408–2414

    Article  PubMed  Google Scholar 

  • Schulz E, Zherdin A, Tiemann L, Plant C, Ploner M (2012) Decoding an individual’s sensitivity to pain from the multivariate analysis of EEG data. Cereb Cortex 22:1118–1123

    Article  PubMed  Google Scholar 

  • Schweinhardt P, Bushnell MC (2010) Pain imaging in health and disease: How far have we come? J Clin Invest 120:3788–3797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Strulov L, Zimmer EZ, Granot M, Tamir A, Jakobi P, Lowenstein L (2007) Pain catastrophizing, response to experimental heat stimuli, and post-cesarean section pain. J Pain 8:273–279

    Article  PubMed  Google Scholar 

  • Tracey I, Mantyh PW (2007) The cerebral signature for pain perception and its modulation. Neuron 55:377–391

    Article  CAS  PubMed  Google Scholar 

  • Valentini E, Hu L, Chakrabarti B, Hu Y, Aglioti SM, Iannetti GD (2012) The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli. Neuroimage 59:1571–1581

    Article  CAS  PubMed  Google Scholar 

  • Willer JC (1977) Comparative study of perceived pain and nociceptive flexion reflex in man. Pain 3:69–80

    Article  CAS  PubMed  Google Scholar 

  • Witting N, Kupers RC, Svensson P, Arendt N, Gjedde A, Jensen TS (2001) Experimental brush-evoked allodynia activates posterior parietal cortex. Neurology 57:1817–1824

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZG, Hu L, Hung YS, Mouraux A, Iannetti GD (2012) Gamma-band oscillations in the primary somatosensory cortex–a direct and obligatory correlate of subjective pain intensity. J Neurosci 32:7429–7438

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the Fonds de Recherche du Québec—Santé (P. G.), the Canadian Institutes of Health Research (S. M., P. G.), the Canada Research Chair program (K. W.), and, the Natural Sciences and Engineering Research Council of Canada (K. W.). We thank all participating volunteers.

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The authors declare that they have no conflict of interest with any of the work presented in this manuscript.

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Correspondence to Philippe Goffaux.

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Goffaux, P., Girard-Tremblay, L., Marchand, S. et al. Individual Differences in Pain Sensitivity Vary as a Function of Precuneus Reactivity. Brain Topogr 27, 366–374 (2014). https://doi.org/10.1007/s10548-013-0291-0

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  • DOI: https://doi.org/10.1007/s10548-013-0291-0

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