Physiological effects of mechanical pain stimulation at the lower back measured by functional near-infrared spectroscopy and capnography

Journal of Integrative NeuroscienceVol. 13, No. 01, pp. 121-142 (2014) ArticlesNo AccessPhysiological effects of mechanical pain stimulation at the lower back measured by functional near-infrared spectroscopy and capnographyLisa Holper, Andrea Gross, Felix Scholkmann, B. Kim Humphreys, Michael L. Meier, Ursula Wolf, Martin Wolf, and Sabina Hotz-BoendermakerLisa HolperBiomedical Optics Research Laboratory (BORL), Division of Neonatology, University Hospital Zurich, Frauenklinikstrasse 10, 8091 Zurich, SwitzerlandCorresponding author., Andrea GrossBiomedical Optics Research Laboratory (BORL), Division of Neonatology, University Hospital Zurich, Frauenklinikstrasse 10, 8091 Zurich, Switzerland, Felix ScholkmannBiomedical Optics Research Laboratory (BORL), Division of Neonatology, University Hospital Zurich, Frauenklinikstrasse 10, 8091 Zurich, Switzerland, B. Kim HumphreysUniversity Hospital Balgrist, Division of Chiropractic Medicine, Forchstrasse 340, 8008 Zurich, Switzerland, Michael L. MeierUniversity Hospital Balgrist, Division of Chiropractic Medicine, Forchstrasse 340, 8008 Zurich, Switzerland, Ursula WolfInstitute for Complementary Medicine IKOM, Inselspital, University of Bern, 3010 Bern, Switzerland, Martin WolfBiomedical Optics Research Laboratory (BORL), Division of Neonatology, University Hospital Zurich, Frauenklinikstrasse 10, 8091 Zurich, Switzerland, and Sabina Hotz-BoendermakerInstitute for Complementary Medicine IKOM, Inselspital, University of Bern, 3010 Bern, Switzerlandhttps://doi.org/10.1142/S0219635214500071Cited by:19 PreviousNext AboutSectionsPDF/EPUB ToolsAdd to favoritesDownload CitationsTrack CitationsRecommend to Library ShareShare onFacebookTwitterLinked InRedditEmail AbstractThe aim was to investigate the effect of mechanical pain stimulation at the lower back on hemodynamic and oxygenation changes in the prefrontal cortex (PFC) assessed by functional near-infrared spectroscopy (fNIRS) and on the partial pressure of end-tidal carbon dioxide (PetCO2) measured by capnography. 13 healthy subjects underwent three measurements (M) during pain stimulation using pressure pain threshold (PPT) at three locations, i.e., the processus spinosus at the level of L4 (M1) and the lumbar paravertebral muscles at the level of L1 on the left (M2) and the right (M3) side. Results showed that only in the M2 condition the pain stimulation elicited characteristic patterns consisting of (1) a fNIRS-derived decrease in oxy- and total hemoglobin concentration and tissue oxygen saturation, an increase in deoxy-hemoglobin concentration, (2) a decrease in the PetCO2 response and (3) a decrease in coherence between fNIRS parameters and PetCO2 responses in the respiratory frequency band (0.2–0.5 Hz). We discuss the comparison between M2 vs. M1 and M3, suggesting that the non-significant findings in the two latter measurements were most likely subject to effects of the different stimulated tissues, the stimulated locations and the stimulation order. We highlight that PetCO2 is a crucial parameter for proper interpretation of fNIRS data in experimental protocols involving pain stimulation. Together, our data suggest that the combined fNIRS-capnography approach has potential for further development as pain monitoring method, such as for evaluating clinical pain treatment.Keywords:Functional near-infrared spectroscopypartial pressure of end-tidal carbon dioxidepain monitoringcoherence analysis References A. Akın and D. Bilensoy, Brain Res. 1107(1), 206 (2006), DOI: 10.1016/j.brainres.2006.06.002. Crossref, Medline, ISI, Google ScholarG. B. Andersson, Lancet 354(9178), 581 (1999), DOI: 10.1016/S0140-6736(99)01312-4. Crossref, Medline, ISI, Google ScholarA. Azar, IEEE Eng. Med. Biol. Soc. 2009, 1375 (2009). Google ScholarM. N. Balikiet al., The J. Neurosci. 26(47), 12165 (2006), DOI: 10.1523/JNEUROSCI.3576-06.2006. Crossref, Medline, ISI, Google ScholarP. A. Bandettini and E. C. Wong, NMR Biomed. 10(5), 197 (1997). Crossref, Medline, ISI, Google ScholarZ. Baratiet al., Ann. Biomed. Eng. 41(2), 223 (2013), DOI: 10.1007/s10439-012-0642-0. Crossref, Medline, ISI, Google ScholarM. Bartocciet al., Pain 122(2), 109 (2006), DOI: 10.1016/j.pain.2006.01.015. Crossref, Medline, ISI, Google ScholarL. Becerraet al., PLoS ONE 4(11), e8016 (2009), DOI: 10.1371/journal.pone.0008016. Crossref, Medline, Google ScholarC. N. Bernsteinet al., Am. J. Gastroenterol. 97(2), 319 (2002), DOI: 10.1111/j.1572-0241.2002.05464.x. Crossref, Medline, ISI, Google ScholarM. Biallaset al., J. Biomed. Opt. 17(8), 086011 (2012). Medline, Google ScholarR. M. Birnet al., NeuroImage 31(4), 1536 (2006), DOI: 10.1016/j.neuroimage.2006.02.048. Crossref, Medline, ISI, Google ScholarB. Biswalet al., Time-frequency analysis of functional EPI time-course series, Proceedings Society of Magnetic Resonance in Medicine, 12th Annual Meeting (1993) p. 722. Google ScholarK. Bornhövdet al., Brain 125(6), 1326 (2002). Crossref, Medline, ISI, Google ScholarK. L. Casey, Proc. Natl. Acad. Sci. 96(14), 7668 (1999), DOI: 10.1073/pnas.96.14.7668. Crossref, Medline, ISI, Google ScholarC. Chang and G. H. Glover, NeuroImage 47(4), 1381 (2009), DOI: 10.1016/j.neuroimage.2009.04.048. Crossref, Medline, ISI, Google ScholarJ. Choiet al., J. Biomed. Opt. 9(1), 221 (2004), DOI: 10.1117/1.1628242. Crossref, Medline, ISI, Google ScholarR. C. Coghillet al., J. Neurophysiol. 82(4), 1934 (1999). Crossref, Medline, ISI, Google ScholarR. Cooperet al., Front. Neurosci. 6, 147 (2012), DOI: 10.3389/fnins.2012.00147. Medline, ISI, Google ScholarD. Cordeset al., Am. J. Neuroradiol. 22(7), 1326 (2001). Medline, ISI, Google ScholarR. A. Deyo, S. K. Mirza and B. I. Martin, Spine 31(23), 2724 (2006), DOI: 10.1097/01.brs.0000244618.06877.cd. Crossref, Medline, ISI, Google ScholarL. Dommeret al., Behav. Brain Res. 234(2), 212 (2012), DOI: 10.1016/j.bbr.2012.06.024. Crossref, Medline, ISI, Google ScholarA. Dubois, A. Britt and W. Fenn, J. Appl. Phys. 4(7), 535 (1952). Google ScholarA. J. Fallgatter, T. J. Muller and W. K. Strik, Neuropsychobiology 37, 215 (1998), DOI: 10.1159/000026506. Crossref, Medline, ISI, Google ScholarJ. Fanget al., Evid.-Based Complement. Altern. Med. 2012, 11 (2012). Google ScholarM. Franceschiniet al., Appl. Opt. 37(31), 7447 (1998), DOI: 10.1364/AO.37.007447. Crossref, Medline, ISI, Google ScholarU. Friebel, S. B. Eickhoff and M. Lotze, NeuroImage 58(4), 1070 (2011), DOI: 10.1016/j.neuroimage.2011.07.022. Crossref, Medline, ISI, Google ScholarC. Gélinaset al., J. Crit. Care 39(6), 485 (2010). Google ScholarA. Grinsted, J. Moore and S. Jevrejeva, Nonlinear Process. Geophys. 11, 561 (2004), DOI: 10.5194/npg-11-561-2004. Crossref, ISI, Google ScholarF. Haeussingeret al., PLoS ONE 6(10), e26377 (2011), DOI: 10.1371/journal.pone.0026377. Crossref, Medline, Google ScholarJ. A. Hashmiet al., Brain 136(9), 2751 (2013), DOI: 10.1093/brain/awt211. Crossref, Medline, ISI, Google Scholar D. Hess et al. , Respiratory Care: Principles and Practice ( Jones & Bartlett Learning , 2011 ) . Google ScholarL. Holperet al., Cortex 48(5), 593 (2012), DOI: 10.1016/j.cortex.2011.02.001. Crossref, Medline, ISI, Google ScholarL. Holper, F. Scholkmann and M. Wolf, NeuroImage 63(1), 212 (2012), DOI: 10.1016/j.neuroimage.2012.06.028. Crossref, Medline, ISI, Google ScholarE. Horiet al., Autonom. Neurosci. 157(2), 74 (2010), DOI: 10.1016/j.autneu.2010.06.007. Crossref, Medline, ISI, Google ScholarD. Hueberet al., Opt. Tomogr. Spectrosc. Tissue III: Proc. SPIE 3597, 618 (1999), DOI: 10.1117/12.356784. Crossref, Google ScholarT. J. Huppertet al., J. Cereb. Blood Flow Metab. 27(6), 1262 (2007), DOI: 10.1038/sj.jcbfm.9600435. Crossref, Medline, ISI, Google ScholarT. J. Huppertet al., NeuroImage 29(2), 368 (2006), DOI: 10.1016/j.neuroimage.2005.08.065. Crossref, Medline, ISI, Google ScholarH. Jaspers, Electroencephalogr. Clin. Neurophysiol. 10, 371 (1958). Google ScholarP. Jezzardet al., An investigation of the contribution of physiological noise in human functional MRI studies at 1.5 tesla and 4 tesla, Proceedings Society of Magnetic Resonance in Medicine, 12th Annual Meeting (1993) p. 1392. Google ScholarG. Ji and V. Neugebauer, J. Neurophysiol. 106(5), 2642 (2011), DOI: 10.1152/jn.00461.2011. Crossref, Medline, ISI, Google ScholarG. Jiet al., J. Neurosci. 30(15), 5451 (2010), DOI: 10.1523/JNEUROSCI.0225-10.2010. Crossref, Medline, ISI, Google ScholarY. Kobayashiet al., Spine 34(22), 2431 (2009), DOI: 10.1097/BRS.0b013e3181b1fb76. Crossref, Medline, Google ScholarJ. Konget al., Pain 148(2), 257 (2010), DOI: 10.1016/j.pain.2009.11.008. Crossref, Medline, ISI, Google Scholar Krishnamurthy, V. (2010) Investigation of neural correlates between perception of pain and hemodynamic response measured in the pre-frontal cortex using functional near infra-red spectroscopy. The University of Texas at Arlington . Google ScholarT.-Q. Liet al., NeuroImage 9(2), 243 (1999), DOI: 10.1006/nimg.1998.0399. Crossref, Medline, ISI, Google ScholarJ. Lorenz, S. Minoshima and K. L. Casey, Brain 126(5), 1079 (2003), DOI: 10.1093/brain/awg102. Crossref, Medline, ISI, Google ScholarC.-M. Luet al., J. Neurosci. Meth. 186(2), 242 (2010), DOI: 10.1016/j.jneumeth.2009.11.010. Crossref, Medline, ISI, Google Scholar Meier, M.L., Hotz-Boendermaker, S., Boendermaker, B., Luechinger, R. & Humphreys, B.K. (2014) Neural responses of posterior to anterior movement on lumbar vertebrae: A functional magnetic resonance imaging study. WFC Award Winning Papers, 37(1), 32–41 . Google ScholarE. Okada and D. Delpy, Appl. Opt. 42(16), 2915 (2003), DOI: 10.1364/AO.42.002915. Crossref, Medline, ISI, Google ScholarA. Park, Time 177(9), 64 (2001). Medline, Google ScholarR. Peyronet al., Brain 122(9), 1765 (1999), DOI: 10.1093/brain/122.9.1765. Crossref, Medline, ISI, Google ScholarR. Peyron, B. Laurent and L. García-Larrea, Clin. Neurophysiol. 30(5), 263 (2000), DOI: 10.1016/S0987-7053(00)00227-6. Crossref, ISI, Google ScholarG. Pfurtschelleret al., Int. J. Psychophysiol. 76(3), 186 (2010), DOI: 10.1016/j.ijpsycho.2010.03.013. Crossref, Medline, ISI, Google ScholarC. Pinnegar and L. Mansinha, Geophysics 68(1), 381 (2003), DOI: 10.1190/1.1543223. Crossref, ISI, Google ScholarM. Rangeret al., Pain Res. Manage. 16(5), 331 (2011). Crossref, Medline, ISI, Google ScholarP. Robbinset al., J. Appl. Phys. 68(4), 1727 (1990). ISI, Google ScholarE. Rostrupet al., NeuroImage 11(2), 87 (2000), DOI: 10.1006/nimg.1999.0526. Crossref, Medline, ISI, Google ScholarE. Sartonet al., Anesthesiology 87(2), 289 (1997), DOI: 10.1097/00000542-199708000-00016. Crossref, Medline, ISI, Google ScholarS. Savaet al., Mol. Pain 5(1), 30 (2009), DOI: 10.1186/1744-8069-5-30. Crossref, Medline, ISI, Google ScholarP. Schenk, T. Laeubli and A. Klipstein, Eur. Spine J. 16(2), 267 (2007), DOI: 10.1007/s00586-006-0124-x. Crossref, Medline, ISI, Google ScholarF. Scholkmann, J. Boss and M. Wolf, Algorithms 5(4), 588 (2012), DOI: 10.3390/a5040588. Crossref, Google ScholarF. Scholkmannet al., NeuroImage 66, 71 (2013), DOI: 10.1016/j.neuroimage.2012.10.025. Crossref, Medline, ISI, Google ScholarF. Scholkmannet al., J. Biomed. Opt. 19(1), 17002 (2014), DOI: 10.1117/1.JBO.19.1.017002. Crossref, Medline, ISI, Google ScholarF. Scholkmannet al., Physiol. Meas. 31(5), 649 (2010), DOI: 10.1088/0967-3334/31/5/004. Crossref, Medline, ISI, Google ScholarR. Slateret al., PLoS Med 5(6), e129 (2008), DOI: 10.1371/journal.pmed.0050129. Crossref, Medline, Google ScholarR. Slateret al., J. Neurosci. 26(14), 3662 (2006), DOI: 10.1523/JNEUROSCI.0348-06.2006. Crossref, Medline, ISI, Google ScholarM. Smithet al., J. Manipulative Physiol. Ther. 36(1), 2 (2013), DOI: 10.1016/j.jmpt.2012.12.001. Crossref, Medline, ISI, Google ScholarJ. C. Széles and G. Litscher, Neurol. Res. 26(7), 797 (2004), DOI: 10.1179/016164104225016100. Crossref, Medline, ISI, Google ScholarP. Terekhin and C. Forster, Neurosci. Lett. 400(2), 110 (2006), DOI: 10.1016/j.neulet.2006.02.040. Crossref, Medline, ISI, Google ScholarC. Torrence and G. Compo, Bull. Am. Meteorol. Soc. 79, 61 (1998). Crossref, ISI, Google ScholarA. Veselyet al., Magn. Reson. Med. 45(6), 1011 (2001), DOI: 10.1002/mrm.1134. Crossref, Medline, ISI, Google ScholarS. Violaet al., Neurol. Sci. 31(1), S165 (2010), DOI: 10.1007/s10072-010-0318-1. Crossref, Medline, Google ScholarD. Ward and S. Karan, J. Anesth. 16(3), 216 (2002), DOI: 10.1007/s005400200028. Crossref, Medline, Google ScholarY. Watanabeet al., Neurosci. Res. 69(1), 60 (2011), DOI: 10.1016/j.neures.2010.09.003. Crossref, Medline, ISI, Google ScholarR. Weisskoffet al., Power spectrum analysis of functionally-weighted MR data: What's in the noise?, Proceedings Society of Magnetic Resonance in Medicine, 12th Annual Meeting (1993) p. 7. Google ScholarR. Wenzelet al., J. Cereb. Blood Flow Metab. 20(7), 1103 (2000). Crossref, Medline, ISI, Google ScholarJ. West, Am. Rev. Respir. Dis. 116(5), 919 (1977). Medline, ISI, Google ScholarB. R. Whiteet al., NeuroImage 47(1), 148 (2009), DOI: 10.1016/j.neuroimage.2009.03.058. Crossref, Medline, ISI, Google ScholarK. Wiechet al., J. Neurosci. 26(44), 11501 (2006), DOI: 10.1523/JNEUROSCI.2568-06.2006. Crossref, Medline, ISI, Google ScholarF. Wilhelm, R. Gevirtz and W. Roth, Behav. Mod. 25, 513 (2001), DOI: 10.1177/0145445501254003. Crossref, Medline, ISI, Google ScholarR. G. Wiseet al., NeuroImage 21(4), 1652 (2004), DOI: 10.1016/j.neuroimage.2003.11.025. Crossref, Medline, ISI, Google ScholarR. G. Wiseet al., J. Cerebral Blood Flow Metab. 27(8), 1521 (2007), DOI: 10.1038/sj.jcbfm.9600465. Crossref, Medline, ISI, Google ScholarU. Wolfet al., Sci. World J. 11, 1206 (2011), DOI: 10.1100/tsw.2011.116. Crossref, ISI, Google ScholarH. Yasuiet al., Autonom. Neurosci. 156(2), 96 (2010), DOI: 10.1016/j.autneu.2010.03.011. Crossref, Medline, ISI, Google ScholarA. Yennuet al., J. Appl. Biobehav. Res. 18(3), 134 (2013), DOI: 10.1111/jabr.12009. Crossref, Google Scholar FiguresReferencesRelatedDetailsCited By 19Systemic physiology augmented functional near-infrared spectroscopy: a powerful approach to study the embodied human brainFelix Scholkmann, Ilias Tachtsidis, Martin Wolf and Ursula Wolf1 Jul 2022 | Neurophotonics, Vol. 9, No. 03Preliminary study: quantification of chronic pain from physiological dataZhuowei Cheng, Franklin Ly, Tyler Santander, Elyes Turki and Yun Zhao et al.1 November 2022 | PAIN Reports, Vol. 7, No. 6Shedding light on pain for the clinic: a comprehensive review of using functional near-infrared spectroscopy to monitor its process in the brainXiao-Su Hu, Thiago D. Nascimento and Alexandre F. DaSilva5 April 2021 | Pain, Vol. 162, No. 12Evaluation of fNIRS signal components elicited by cognitive and hypercapnic stimuliPratusha Reddy, Meltem Izzetoglu, Patricia A. Shewokis, Michael Sangobowale and Ramon Diaz-Arrastia et al.6 December 2021 | Scientific Reports, Vol. 11, No. 1Pain Induced Changes in Brain Oxyhemoglobin: A Systematic Review and Meta-Analysis of Functional NIRS StudiesMacGregor Hall, Dawson Kidgell, Luke Perraton, Jack Morrissey and Shapour Jaberzadeh28 February 2021 | Pain Medicine, Vol. 22, No. 6Multivariate analysis of the systemic response to auditory stimulation: An integrative approachManuel Muñoz‐Caracuel, Vanesa Muñoz, Francisco J. Ruíz‐Martínez, Dalila Di Domenico and Sabrina Brigadoi et al.10 March 2021 | Experimental Physiology, Vol. 106, No. 4NIRS measures in pain and analgesia: Fundamentals, features, and functionKeerthana Deepti Karunakaran, Ke Peng, Delany Berry, Stephen Green and Robert Labadie et al.1 Jan 2021 | Neuroscience & Biobehavioral Reviews, Vol. 120Dynamic interpersonal neural synchronization underlying pain‐induced cooperation in femalesChenbo Wang, Tingyu Zhang, Zhoukuidong Shan, Jieqiong Liu and Di Yuan et al.4 April 2019 | Human Brain Mapping, Vol. 40, No. 11Applications of Functional Near-Infrared Spectroscopy (fNIRS) Neuroimaging in Exercise–Cognition Science: A Systematic, Methodology-Focused ReviewFabian Herold, Patrick Wiegel, Felix Scholkmann and Notger Müller22 November 2018 | Journal of Clinical Medicine, Vol. 7, No. 12Morphine Attenuates fNIRS Signal Associated With Painful Stimuli in the Medial Frontopolar Cortex (medial BA 10)Ke Peng, Meryem A. Yücel, Sarah C. Steele, Edward A. Bittner and Christopher M. Aasted et al.4 October 2018 | Frontiers in Human Neuroscience, Vol. 12Brodmann area 10: Collating, integrating and high level processing of nociception and painKe Peng, Sarah C. Steele, Lino Becerra and David Borsook1 Feb 2018 | Progress in Neurobiology, Vol. 161Characterization of the functional near-infrared spectroscopy response to nociception in a pediatric populationVanessa A. Olbrecht, Yifei Jiang, Luigi Viola, Charlotte M. Walter and Hanli Liu et al.27 December 2017 | Pediatric Anesthesia, Vol. 28, No. 2Using prerecorded hemodynamic response functions in detecting prefrontal pain response: a functional near-infrared spectroscopy studyKe Peng, Meryem A. Yücel, Christopher M. Aasted, Sarah C. Steele and David A. Boas et al.1 Jan 2018 | Neurophotonics, Vol. 5, No. 01Prefrontal hemodynamic mapping by functional near-infrared spectroscopy in response to thermal stimulations over three body sitesAmarnath Yennu, Fenghua Tian, Robert J. Gatchel and Hanli Liu19 Dec 2016 | Neurophotonics, Vol. 3, No. 4Different mechanosensory stimulations of the lower back elicit specific changes in hemodynamics and oxygenation in cortical sensorimotor areas—A fNIRS studyAndrea Vrana, Michael L. Meier, Sabina Hotz‐Boendermaker, Barry K. Humphreys and Felix Scholkmann14 October 2016 | Brain and Behavior, Vol. 6, No. 12Cortical Sensorimotor Processing of Painful Pressure in Patients with Chronic Lower Back Pain—An Optical Neuroimaging Study using fNIRSAndrea Vrana, Michael L. Meier, Sabina Hotz-Boendermaker, Barry K. Humphreys and Felix Scholkmann17 November 2016 | Frontiers in Human Neuroscience, Vol. 10Time–frequency dynamics of the sum of intra- and extracerebral hemodynamic functional connectivity during resting-state and respiratory challenges assessed by multimodal functional near-infrared spectroscopyL. Holper, F. Scholkmann and E. Seifritz1 Oct 2015 | NeuroImage, Vol. 120Specificity of Hemodynamic Brain Responses to Painful Stimuli: A functional near-infrared spectroscopy studyMeryem A. Yücel, Christopher M. Aasted, Mihayl P. Petkov, David Borsook and David A. Boas et al.30 March 2015 | Scientific Reports, Vol. 5, No. 1Artifact reduction in long-term monitoring of cerebral hemodynamics using near-infrared spectroscopySarah A. Vinette, Jeff F. Dunn, Edward Slone and Paolo Federico26 May 2015 | Neurophotonics, Vol. 2, No. 2 Recommended Vol. 13, No. 01 Metrics History Received 12 December 2013 Accepted 10 February 2014 Published: 21 March 2014 KeywordsFunctional near-infrared spectroscopypartial pressure of end-tidal carbon dioxidepain monitoringcoherence analysisPDF download