Neuroimaging-based biomarkers for pain: state of the field and current directions

Maite M van der Miesen, Martin A Lindquist, Tor D Wager, Maite M van der Miesen, Martin A Lindquist, Tor D Wager

Abstract

Chronic pain is an endemic problem involving both peripheral and brain pathophysiology. Although biomarkers have revolutionized many areas of medicine, biomarkers for pain have remained controversial and relatively underdeveloped. With the realization that biomarkers can reveal pain-causing mechanisms of disease in brain circuits and in the periphery, this situation is poised to change. In particular, brain pathophysiology may be diagnosable with human brain imaging, particularly when imaging is combined with machine learning techniques designed to identify predictive measures embedded in complex data sets. In this review, we explicate the need for brain-based biomarkers for pain, some of their potential uses, and some of the most popular machine learning approaches that have been brought to bear. Then, we evaluate the current state of pain biomarkers developed with several commonly used methods, including structural magnetic resonance imaging, functional magnetic resonance imaging and electroencephalography. The field is in the early stages of biomarker development, but these complementary methodologies have already produced some encouraging predictive models that must be tested more extensively across laboratories and clinical populations.

Keywords: Biomarkers; EEG; MRI; MVPA; Machine learning; Neuroimaging; Pain.

Conflict of interest statement

Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.

Copyright © 2019 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of The International Association for the Study of Pain.

Figures

Figure 1.
Figure 1.
Timeline of machine learning articles for pain: a timeline showing the number of published articles per neuroimaging technique or combinations of techniques for pain studies investigating biomarkers (47 in total). Studies include the use of EEG, task fMRI (denoted fMRI), rs-fMRI, sMRI, or a combination of techniques (denoted combined) and use a cross-validation method for their predictive model. EEG, electroencephalography; fMRI, functional magnetic resonance imaging; rs-fMRI, resting-state functional magnetic resonance imaging; sMRI, structural magnetic resonance imaging.

References

    1. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 2005;9:463–84.
    1. Apkarian AV, Sosa Y, Krauss BR, Thomas PS, Fredrickson BE, Levy RE, Harden RN, Chialvo DR. Chronic pain patients are impaired on an emotional decision-making task. PAIN 2004;108:129–36.
    1. Baber Z, Erdek MA. Failed back surgery syndrome: current perspectives. J Pain Res 2016:979–87.
    1. Bagarinao E, Johnson KA, Martucci KT, Ichesco E, Farmer MA, Labus J, Ness TJ, Harris R, Deutsch G, Apkarian AV, Mayer EA, Clauw DJ, Mackey S. Preliminary structural MRI based brain classification of chronic pelvic pain: a MAPP network study. PAIN 2014;155:2502–9.
    1. Bai Y, Huang G, Tu Y, Tan A, Hung YS, Zhang Z. Normalization of pain-evoked neural responses using spontaneous EEG improves the performance of EEG-based cross-individual pain prediction. Front Comput Neurosci 2016;10:1–10.
    1. Baliki MN, Geha PY, Fields HL, Apkarian AV. Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain. Neuron 2010;66:149–60.
    1. Baliki MN, Petre B, Torbey S, Herrmann KM, Huang L, Schnitzer TJ, Fields HL, Apkarian AV. Corticostriatal functional connectivity predicts transition to chronic back pain. Nat Neurosci 2012;15:1117–19.
    1. Becker S, Gandhi W, Pomares F, Wager TD, Schweinhardt P. Orbitofrontal cortex mediates pain inhibition by monetary reward. Soc Cogn Affect Neurosci 2017;12:651–61.
    1. Boissoneault J, Sevel L, Letzen J, Robinson M, Staud R. Biomarkers for musculoskeletal pain conditions: use of brain imaging and machine learning. Curr Rheumatol Rep 2017;19:5.
    1. Bosma RL, Cheng JC, Rogachov A, Kim JA, Hemington KS, Osborne NR, Raghavan LV, Bhatia A, Davis KD. Brain dynamics and temporal summation of pain predicts neuropathic pain relief from ketamine infusion. Anesthesiology 2018;129:1015–24.
    1. Bräscher AK, Becker S, Hoeppli ME, Schweinhardt P. Different brain circuitries mediating controllable and uncontrollable pain. J Neurosci 2016;36:5013–25.
    1. Brodersen KH, Wiech K, Lomakina EI, Lin CS, Buhmann JM, Bingel U, Ploner M, Stephan KE, Tracey I. Decoding the perception of pain from fMRI using multivariate pattern analysis. Neuroimage 2012;63:1162–70.
    1. Brown JE, Chatterjee N, Younger J, Mackey S. Towards a physiology-based measure of pain: patterns of human brain activity distinguish painful from non-painful thermal stimulation. PLoS One 2011;6:2–9.
    1. Bushnell MC, Čeko M, Low LA. Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 2013;14:502–11.
    1. Callan D, Mills L, Nott C, England R, England S. A tool for classifying individuals with chronic back pain: using multivariate pattern analysis with functional magnetic resonance imaging data. PLoS One 2014;9:e98007.
    1. Carlino E, Frisaldi E, Benedetti F. Pain and the context. Nat Rev Rheumatol 2014;10:348–55.
    1. Carragee EJ, Alamin TF, Carragee JM. Low-pressure positive discography in subjects asymptomatic of significant low back pain illness. Spine (Phila Pa 1976) 2006;31:505–9.
    1. Carragee EJ, Alamin TF, Miller JL, Carragee JM. Discographic, MRI and psychosocial determinants of low back pain disability and remission: a prospective study in subjects with benign persistent back pain. Spine J 2005;5:24–35.
    1. Carrasquillo Y, Gereau RW. Activation of the extracellular signal-regulated kinase in the amygdala modulates pain perception. J Neurosci 2007;27:1543–51.
    1. Cecchi GA, Huang L, Hashmi JA, Baliki M, Centeno MV, Rish I, Apkarian AV. Predictive dynamics of human pain perception. PLoS Comput Biol 2012;8:e1002719.
    1. Chang LJ, Gianaros PJ, Manuck SB, Krishnan A. A sensitive and specific neural signature for picture-induced negative affect. PLoS Biol 2015;13:e1002180.
    1. Chen T, Mu J, Xue Q, Yang L, Dun W, Zhang M, Liu J. Whole-brain structural magnetic resonance imaging—based classification of primary dysmenorrhea in pain-free phase: a machine learning study. PAIN 2019;160:734–41.
    1. Cheng JC, Rogachov A, Hemington KS, Kucyi A, Bosma RL, Lindquist MA, Inman RD, Davis KD. Multivariate machine learning distinguishes cross-network dynamic functional connectivity patterns in state and trait neuropathic pain. PAIN 2018;158:1764–76.
    1. Chong CD, Gaw N, Fu Y, Li J, Wu T, Schwedt TJ. Migraine classification using magnetic resonance imaging resting-state functional connectivity data. Cephalalgia 2017;37:828–44.
    1. Chou R, Atlas SJ, Stanos SP, Rosenquist RW. Nonsurgical interventional therapies for low back pain: a review of the evidence for an American pain society clinical practice guideline. Spine (Phila Pa 1976) 2009;34:1094–1109.
    1. Chyzhyk D, Varoquaux G, Thirion B, Milham M. Controlling a confound in predictive models with a test set minimizing its effect. International Workshop on Pattern Recognition in Neuroimaging, PRNI 2018;2018:1–4.
    1. Corder G, Ahanonu B, Grewe BF, Wang D, Schnitzer MJ, Scherrer G. An amygdalar neural ensemble that encodes the unpleasantness of pain. Science 2019;363:276–81.
    1. Davis KD, Flor H, Greely HT, Iannetti GD, MacKey S, Ploner M, Pustilnik A, Tracey I, Treede RD, Wager TD. Brain imaging tests for chronic pain: medical, legal and ethical issues and recommendations. Nat Rev Neurol 2017;13:624–38.
    1. Denk F, McMahon SB, Tracey I. Pain vulnerability: a neurobiological perspective. Nat Neurosci 2014;17:192–200.
    1. Dinga R, Schmaal L, Penninx B, van Tol MJ, Veltman DJ, van Velzen L, van Der Wee N, Marquand A. Evaluating the evidence for biotypes of depression: attempted replication of Drysdale et al. NeuroImage Clin 2019;22:101796.
    1. Dosenbach NUF, Nardos B, Cohen AL, Fair DA, Power JD, Church JA, Nelson SM, Wig GS, Vogel AC, Lessov-Schlaggar CN, Barnes KA, Dubis JW, Feczko E, Coalson RS, Pruett JR, Jr, Barch DM, Petersen SE, Schlaggar BL. Prediction of individual brain maturity using fMRI. Science 2010;329:1358–61.
    1. Downie AS, Hancock MJ, Rzewuska M, Williams CM, Lin CWC, Maher CG. Trajectories of acute low back pain: a latent class growth analysis. PAIN 2015;157:225–34.
    1. Drysdale AT, Grosenick L, Downar J, Dunlop K, Mansouri F, Meng Y, Fetcho RN, Zebley B, Oathes DJ, Etkin A, Schatzberg AF, Sudheimer K, Keller J, Mayberg HS, Gunning FM, Alexopoulos GS, Fox MD, Pascual-Leone A, Voss HU, Casey BJ, Dubin MJ, Liston C. Resting-state connectivity biomarkers define neurophysiological subtypes of depression. Nat Med 2017;23:28–38.
    1. Duerden EG, Albanese MC. Localization of pain-related brain activation: a meta-analysis of neuroimaging data. Hum Brain Mapp 2013;34:109–49.
    1. Dunn KM, Campbell P, Jordan KP. Long-term trajectories of back pain: cohort study with 7-year follow-up. BMJ Open 2013;3:e003838.
    1. EFIC. Declaration on Pain. Available at: .
    1. Eisenberger NI. Social pain and the brain: controversies, questions, and where to go from here. Annu Rev Psychol 2015;66:601–29.
    1. Fayaz A, Croft P, Langford RM, Donaldson LJ, Jones GT. Prevalence of chronic pain in the UK: a systematic review and meta-analysis of population studies. BMJ Open 2016;6:e010364.
    1. Ferrari M, Quaresima V. A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. Neuroimage 2012;63:921–35.
    1. Finco G, Locci E, Mura P, Massa R, Noto A, Musu M, Landoni G, D'Aloja E, De-Giorgio F, Scano P, Evangelista M. Can urine metabolomics be helpful in differentiating neuropathic and nociceptive pain? A proof-of-concept study. PLoS One 2016;11:e0150476.
    1. Flor H, Turk DC, Scholz OB. Impact of chronic pain on the spouse: marital, emotional and physical consequences. J Psychosom Res 1987;31:63–71.
    1. Freburger JK, Holmes GM, Agans RP, Jackman AM, Darter JD, Wallace AS, Castel LD, Kalsbeek WD, Carey TS. The rising prevalence of chronic low back pain. Arch Intern Med 2009;169:251.
    1. Friebel U, Eickhoff SB, Lotze M. Coordinate-based meta-analysis of experimentally induced and chronic persistent neuropathic pain. Neuroimage 2011;58:1070–80.
    1. Furman AJ, Meeker TJ, Rietschel JC, Yoo S, Muthulingam J, Prokhorenko M, Keaser ML, Goodman RN, Mazaheri A, Seminowicz DA. Cerebral peak alpha frequency predicts individual differences in pain sensitivity. Neuroimage 2018;167:203–10.
    1. Geuter S, Gamer M, Onat S, Büchel C. Parametric trial-by-trial prediction of pain by easily available physiological measures. PAIN 2014;155:994–1001.
    1. Glover GH, Li T, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR Magn Reson Med 2000;44:162–7.
    1. Gram M, Erlenwein J, Petzke F, Falla D, Przemeck M, Emons MI, Reuster M, Olesen SS, Drewes AM. Prediction of postoperative opioid analgesia using clinical-experimental parameters and electroencephalography. Eur J Pain 2017;21:264–77.
    1. Gram M, Graversen C, Olesen AE, Drewes AM. Machine learning on encephalographic activity may predict opioid analgesia. Eur J Pain 2015;19:1552–61.
    1. Graversen C, Olesen SS, Olesen AE, Steimle K, Farina D, Wilder-smith OHG, Bouwense SAW, Van Goor H, Drewes AM. The analgesic effect of pregabalin in patients with chronic pain is reflected by changes in pharmaco-EEG spectral indices. Br J Clin Pharmacol 2011;73:363–72.
    1. Group F-NBW. BEST (biomarkers, endpoints, and other tools) resource. Bethesda: Silver Spring Food Drug Adm (US), Co-published by Natl Institutes Heal (US), 2016.
    1. Group F-NBW. Table of surrogate endpoints that were the basis of drug approval or licensure. 2018. Available at: .
    1. Harper DE, Shah Y, Ichesco E, Gerstner GE, Peltier SJ. Multivariate classification of pain-evoked brain activity in temporomandibular disorder. Pain Rep 2016;1:e572.
    1. Harte SE, Ichesco E, Hampson JP, Peltier SJ, Schmidt-Wilcke T, Clauw DJ, Harris RE. Pharmacologic attenuation of cross-modal sensory augmentation within the chronic pain insula. PAIN 2016;157:1933–45.
    1. Haxby JV. Multivariate pattern analysis of fMRI: the early beginnings. Neuroimage 2012;62:852–5.
    1. Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P. Distributed and overlapping representations of face and objects in ventral temporal cortex. Science 2001;293:2425–31.
    1. Haynes JD, Rees G. Decoding mental states from brain activity in humans. Nat Rev Neurosci 2006;7:523–34.
    1. Hebart MN, Baker CI. Deconstructing multivariate decoding for the study of brain function. Neuroimage 2018;180:4–18.
    1. Huang G, Xiao P, Hung YS, Zhang ZG, Hu L. A novel approach to predict subjective pain perception from single-trial laser-evoked potentials. Neuroimage 2013;81:283–93.
    1. Hung PSP, Chen DQ, Davis KD, Zhong J, Hodaie M. Predicting pain relief: use of pre-surgical trigeminal nerve diffusion metrics in trigeminal neuralgia. Neuroimage Clin 2017;15:710–18.
    1. Jepma M, Koban L, van Doorn J, Jones M, Wager TD. Behavioural and neural evidence for self-reinforcing expectancy effects on pain. Nat Hum Behav 2018;2:838–55.
    1. Kamitani Y, Tong F. Decoding the visual and subjective contents of the human brain. Nat Neurosci 2005;8:679–85.
    1. Kay KN, Naselaris T, Prenger RJ, Gallant JL. Identifying natural images from human brain activity. Nature 2008;452:352–5.
    1. Kongsted A, Kent P, Axen I, Downie AS, Dunn KM. What have we learned from ten years of trajectory research in low back pain? BMC Musculoskelet Disord 2016;17:220.
    1. Kongsted A, Kent P, Hestbaek L, Vach W. Patients with low back pain had distinct clinical course patterns that were typically neither complete recovery nor constant pain. A latent class analysis of longitudinal data. Spine J 2015;15:885–94.
    1. Kragel PA, Koban L, Barrett LF, Wager TD. Review representation, pattern information, and brain Signatures : from neurons to neuroimaging. Neuron 2018;99:257–73.
    1. Kriegeskorte N. Pattern-information analysis: from stimulus decoding to computational-model testing. Neuroimage 2011;56:411–21.
    1. Krishnan A, Woo CW, Chang LJ, Ruzic L, Gu X, López-Solà M, Jackson PL, Pujo J, Fan J, Wager TD. Somatic and vicarious pain are represented by dissociable multivariate brain patterns. Elife 2016;5:e15166.
    1. Kross E, Berman MG, Mischel W, Smith EE, Wager TD. Social rejection shares somatosensory representations with physical pain. Proc Natl Acad Sci U S A 2011;108:6270–5.
    1. Kuner R, Flor H. Structural plasticity and reorganisation in chronic pain. Nat Rev Neurosci 2016;18:20–30.
    1. Kuo PC, Chen YT, Chen YS, Chen LF. Decoding the perception of endogenous pain from resting-state MEG. Neuroimage 2017;144:1–11.
    1. Kutch JJ, Labus JS, Harris RE, Martucci KT, Farmer MA, Fenske S, Fling C, Ichesco E, Peltier S, Petre B, Guo W, Hou X, Stephens AJ, Mullins C, Clauw DJ, Mackey SC, Apkarian AV, Landis JR, Mayer EA. Resting-state functional connectivity predicts longitudinal pain symptom change in urologic chronic pelvic pain syndrome: a MAPP network study. PAIN 2017;158:1069–82.
    1. Labus JS, Van Horn JD, Gupta A, Alaverdyan M, Torgerson C, Ashe-McNalley C, Irimia A, Hong JY, Naliboff B, Tillisch K, Mayer EA. Multivariate morphological brain signatures predict patients with chronic abdominal pain from healthy control subjects. PAIN 2015;156:1545–54.
    1. Labus JS, Naliboff B, Kilpatrick L, Liu C, Ashe-McNalley C, Dos Santos IR, Alaverdyan M, Woodworth D, Gupta A, Ellingson BM, Tillisch K, Mayer EA. Pain and Interoception Imaging Network (PAIN): a multimodal, multisite, brain-imaging repository for chronic somatic and visceral pain disorders. Neuroimage 2017;124:1232–7.
    1. Lancaster J, Mano H, Callan D, Kawato M, Seymour B. Decoding acute pain with combined EEG and physiological data. International IEEE/EMBS Conference Neural Engineering (NER) 2017:521–4.
    1. Lee J, Mawla I, Kim J, Loggia ML, Ortiz A, Jung C, Chan ST, Gerber J, Schmithorst VJ, Edwards RR, Wasan AD, Berna C, Kong J, Kaptchuk TJ, Gollub RL, Rosen BR, Napadow V. Machine learning-based prediction of clinical pain using multimodal neuroimaging and autonomic metrics. PAIN 2019;160:550–60.
    1. Lee M, Manders TR, Eberle SE, Su C, D'amour J, Yang R, Lin HY, Deisseroth K, Froemke RC, Wang J. Activation of corticostriatal circuitry relieves chronic neuropathic pain. J Neurosci 2015;35:5247–59.
    1. Li D, Puntillo K, Miaskowski C. A review of objective pain measures for use with critical care adult patients unable to self-report. J Pain 2008;9:2–10.
    1. Li L, Huang G, Lin Q, Liu J, Zhang S, Zhang Z. Magnitude and temporal variability of inter-stimulus EEG modulate the linear relationship between laser-evoked potentials and fast-pain perception. Front Neurosci 2018;12:1–9.
    1. Liang M, Mouraux A, Hu L, Iannetti GD. Primary sensory cortices contain distinguishable spatial patterns of activity for each sense. Nat Commun 2013;4:1979.
    1. Liu P, Qin W, Wang J, Zeng F, Zhou G, Wen H, von Deneen KM, Liang F, Gong Q, Tian J. Identifying neural patterns of functional dyspepsia using multivariate pattern analysis: a resting-state fMRI study. PLoS One 2013;8:e68205.
    1. Liu Y, Latremoliere A, Li X, Zhang Z, Chen M, Wang X, Fang C, Zhu J, Alexandre C, Gao Z, Chen B, Ding X, Zhou J, Zhang Y, Chen C, Wang KH, Woolf CJ, He Z. Touch and tactile neuropathic pain sensitivity are set by corticospinal projections. Nature 2018;561:547–50.
    1. López-Solà M, Koban L, Wager TD. Transforming pain with prosocial meaning. Psychosom Med 2018;80:814–25.
    1. López-Solà M, Pujol J, Wager TD, Garcia-Fontanals A, Blanco-Hinojo L, Garcia-Blanco S, Poca-Dias V, Harrison BJ, Contreras-Rodríguez O, Monfort J, Garcia-Fructuoso F, Deus J. Altered functional magnetic resonance imaging responses to nonpainful sensory stimulation in fibromyalgia patients. Arthritis Rheumatol 2014;66:3200–9.
    1. López-Solà M, Woo CW, Pujol J, Deus J, Harrison BJ, Monfort J, Wager TD. Towards a neurophysiological signature for fibromyalgia. PAIN 2017;158:34–47.
    1. Lötsch J, Ultsch A. Machine learning in pain research. PAIN 2017;159:623–30.
    1. Makowski C, Lepage M, Evans AC. Head motion: the dirty little secret of neuroimaging in psychiatry. J Psychiatry Neurosci 2018;43:180022.
    1. Manchiakanti L, Giordano J, Boswell MV, Fellows B, Manchukonda R, Pampati V. Psychological factors as predictors of opioid abuse and illicit drug use in chronic pain patients. J Opioid Manag 2007;3:89–100.
    1. Mano H, Kotecha G, Leibnitz K, Matsubara T, Nakae A, Shenker N, Shibata M, Voon V, Yoshida W, Lee M, Yanagida T, Kawato M, Rosa MJ, Seymour B. Classification and characterisation of brain network changes in chronic back pain: a multicenter study. Wellcome Open Res 2018;3:19.
    1. Mansour AR, Baliki MN, Huang L, Torbey S, Herrmann KM, Schnitzer TJ, Apkarian AV. Brain white matter structural properties predict transition to chronic pain. PAIN 2013;154:2160–8.
    1. Marquand A, Howard M, Brammer M, Chu C, Coen S, Mourão-Miranda J. Quantitative prediction of subjective pain intensity from whole-brain fMRI data using Gaussian processes. Neuroimage 2010;49:2178–89.
    1. Miller KL, Alfaro-Almagro F, Bangerter NK, Thomas DL, Yacoub E, Xu J, Bartsch AJ, Jbabdi S, Sotiropoulos SN, Andersson JLR, Griffanti L, Douaud G, Okell TW, Weale P, Dragonu I, Garratt S, Hudson S, Collins R, Jenkinson M, Matthews PM, Smith SM. Multimodal population brain imaging in the UK Biobank prospective epidemiological study. Nat Neurosci 2016;19:1523–36.
    1. Misra G, Wang W, Archer DB, Roy A, Coombes SA. Automated classification of pain perception using high-density electroencephalography data. J Neurophysiol 2017;117:786–95.
    1. Mitchell TM, Shinkareva SV, Carlson A, Chang K, Malave VL, Mason RA, Just MA. Associated with the meanings of nouns. Science 2008;320:1191–5.
    1. Mouraux A, Iannetti GD. The search for pain biomarkers in the human brain. Brain 2018;141:3290–307.
    1. Murray CJL, Lopez AD. Measuring the global burden of disease. N Engl J Med 2013;369:448–57.
    1. Muschelli J, Nebel MB, Caffo BS, Barber AD, Pekar JJ, Mostofsky SH. Reduction of motion-related artifacts in resting state fMRI using aCompCor. Neuroimage 2014;96:22–35.
    1. Nan J, Liu J, Li G, Xiong S, Yan X, Yin Q, Zeng F, von Deneen KM, Liang F, Gong Q, Qin W, Tian J. Whole-brain functional connectivity identification of functional dyspepsia. PLoS One 2013;8:e65870.
    1. Naselaris T, Kay KN, Nishimoto S, Gallant JL. Encoding and decoding in fMRI. Neuroimage 2011;56:400–10.
    1. Neugebauer V, Li W, Bird GC, Han JS. The amygdala and persistent pain. Neuroscientist 2004;10:221–34.
    1. O'Muircheartaigh J, Marquand A, Hodkinson DJ, Krause K, Khawaja N, Renton TF, Huggins JP, Vennart W, Williams SCR, Howard MA. Multivariate decoding of cerebral blood flow measures in a clinical model of on-going postsurgical pain. Hum Brain Mapp 2015;36:633–42.
    1. Parker SL, Mendenhall SK, Godil SS, Sivasubramanian P, Cahill K, Ziewacz J, McGirt MJ. Incidence of low back pain after lumbar discectomy for herniated disc and its effect on patient-reported outcomes. Clin Orthop Relat Res 2015;473:1988–99.
    1. Parkes L, Fulcher B, Yücel M, Fornito A. An evaluation of the efficacy, reliability, and sensitivity of motion correction strategies for resting-state functional MRI. Neuroimage 2018;171:415–36.
    1. Pasley BN, David SV, Mesgarani N, Flinker A, Shamma SA, Crone NE, Knight RT, Chang EF. Reconstructing speech from human auditory cortex. PLoS Biol 2012;10:e1001251.
    1. Pineda R, Neil J, Dierker D, Smyser C, Wallendorf M, Kidokoro H, Reynolds L, Rogers C, Mathur A, Van Essen D, Inder T. Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different neonatal intensive care unit environments. J Pediatr 2015;164:1–22.
    1. Ploner M, May ES. EEG and MEG in pain research—current state and future perspectives. PAIN 2018;159:206–211.
    1. Poldrack RA, Baker CI, Durnez J, Gorgolewski KJ, Matthews PM, Munafò MR, Nichols TE, Poline JB, Vul E, Yarkoni T. Scanning the horizon: towards transparent and reproducible neuroimaging research. Nat Rev Neurosci 2017;18:115–26.
    1. Poldrack RA, Barch DM, Mitchell JP, Wager TD, Wagner AD, Devlin JT, Cumba C, Koyejo O, Milham MP. Toward open sharing of task-based fMRI data: the OpenfMRI project. Front Neuroinform 2013;7:1–12.
    1. Pourshoghi A, Zakeri I, Pourrezaei K. Application of functional data analysis in classification and clustering of functional near-infrared spectroscopy signal in response to noxious stimuli. J Biomed Opt 2016;21:101411.
    1. Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 2014;84:320–41.
    1. Prato M, Favilla S, Zanni L, Porro CA, Baraldi P. A regularization algorithm for decoding perceptual temporal profiles from fMRI data. Neuroimage 2011;56:258–67.
    1. Rao A, Monteiro JM, Mourao-Miranda J. Predictive modelling using neuroimaging data in the presence of confounds. Neuroimage 2017;150:23–49.
    1. Ren W, Centeno MV, Berger S, Wu Y, Na X, Liu X, Kondapalli J, Apkarian AV, Martina M, Surmeier DJ. The indirect pathway of the nucleus accumbens shell amplifies neuropathic pain. Nat Neurosci 2016;19:220–2.
    1. Robinson ME, O'Shea AM, Craggs J, Price DD, Letzen JE, Staud R. Comparison of machine classification algorithms for fibromyalgia: neuroimages versus self-report. J Pain 2015;16:472–77.
    1. Rogachov A, Cheng JC, Hemington KS, Bosma RL, Kim J, Osborne NR, Inman RD, Davis KD. Abnormal low-frequency oscillations reflect trait-like pain ratings in chronic pain patients revealed through a machine learning approach. J Neurosci 2018;38:7293–302.
    1. Rojas RF, Huang X, Ou K. Toward a functional near-infrared spectroscopy-based monitoring of pain assessment for nonverbal patients. J Biomed Opt 2017;22:106013.
    1. Rosa MJ, Seymour B. Decoding the matrix: benefits and limitations of applying machine learning algorithms to pain neuroimaging. PAIN 2014;155:864–7.
    1. Rosenberg MD, Finn ES, Scheinost D, Papademetris X, Shen X, Constable RT, Chun MM. A neuromarker of sustained attention from whole-brain functional connectivity. Nat Neurosci 2015;19:165–71.
    1. Satterthwaite TD, Elliott MA, Gerraty RT, Ruparel K, Loughead J, Calkins ME, Eickhoff SB, Hakonarson H, Gur RE, Wolf DH, Gur RC. An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 2013;64:240–56.
    1. Schnakers C, Zasler ND. Pain assessment and management in disorders of consciousness. Curr Opin Neurol 2007;20:620–6.
    1. Schuller B, Batliner A, Steidl S, Seppi D. Recognising realistic emotions and affect in speech: state of the art and lessons learnt from the first challenge. Speech Commun 2011;53:1062–87.
    1. Schuller B, Steidl S, Batliner A. The INTERSPEECH 2009 emotion challenge. Proceedings Annual Conference of the International Speech Communication Association, INTERSPEECH 2009:312–15.
    1. Schulz E, Zherdin A, Tiemann L, Plant C, Ploner M. Decoding an individual's sensitivity to pain from the multivariate analysis of EEG data. Cereb Cortex 2012;22:1118–23.
    1. Schwartz N, Temkin P, Jurado S, Lim BK, Heifets BD, Polepalli JS, Malenka RC. Decreased motivation during chronic pain requires long-term depression in the nucleus accumbens. Science 2014;345:535–42.
    1. Schwedt TJ, Chong CD, Wu T, Gaw N, Fu Y, Li J. Accurate classification of chronic migraine via brain magnetic resonance imaging. Headache 2015;55:762–77.
    1. Seminowicz DA, Laferriere AL, Millecamps M, Yu JSC, Coderre TJ, Bushnell MC. MRI structural brain changes associated with sensory and emotional function in a rat model of long-term neuropathic pain. Neuroimage 2009;47:1007–14.
    1. Skolasky RL, Wegener ST, Maggard AM, Riley LH. The impact of reduction of pain after lumbar spine surgery: the relationship between changes in pain and physical function and disability. Spine (Phila Pa 1976) 2014;39:1426–32.
    1. Smith A, López-Solà M, McMahon K, Pedler A, Sterling M. Multivariate pattern analysis utilizing structural or functional MRI—in individuals with musculoskeletal pain and healthy controls: a systematic review. Semin Arthritis Rheum 2017;47:418–31.
    1. Snoek L, Miletić S, Scholte HS. How to control for confounds in decoding analyses of neuroimaging data. Neuroimage 2019;184:741–60.
    1. Sokil MB, Lyashuk OL, Dovbush AP. ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. INMATEH Agric Eng 2016;48:119–24.
    1. Sundermann B, Burgmer M, Pogatzki-Zahn E, Gaubitz M, Stüber C, Wessolleck E, Heuft G, Pfleiderer B. Diagnostic classification based on functional connectivity in chronic pain: model optimization in fibromyalgia and rheumatoid arthritis. Acad Radiol 2014;21:369–77.
    1. Tan LL, Pelzer P, Heinl C, Tang W, Gangadharan V, Flor H, Sprengel R, Kuner T, Kuner R. A pathway from midcingulate cortex to posterior insula gates nociceptive hypersensitivity. Nat Neurosci 2017;20:1591–601.
    1. Tétreault P, Mansour A, Vachon-Presseau E, Schnitzer TJ, Apkarian AV, Baliki MN. Brain connectivity predicts placebo response across chronic pain clinical trials. PLoS Biol 2016;14:e1002570.
    1. Todd MT, Nystrom LE, Cohen JD. Confounds in multivariate pattern analysis: theory and rule representation case study. Neuroimage 2013;77:157–65.
    1. Tracey I, Bushnell MC. How neuroimaging studies have challenged us to rethink: is chronic pain a disease? J Pain 2009;10:1113–20.
    1. Tracey I, Johns E. The pain matrix: reloaded or reborn as we image tonic pain using arterial spin labelling. PAIN 2010;148:359–60.
    1. Tracey I, Mantyh PW. The cerebral signature for pain perception and its modulation. Neuron 2007;55:377–91.
    1. Tu Y, Tan A, Bai Y, Hung YS, Zhang Z. Decoding subjective intensity of nociceptive pain from pre-stimulus and post-stimulus brain activities. Front Comput Neurosci 2016;10:1–11.
    1. Tu YH, Fu ZN, Tan A, Huang G, Hu L, Hung YS, Zhang ZG. A novel and effective fMRI decoding approach based on sliced inverse regression and its application to pain prediction. Neurocomputing 2018;273:373–84.
    1. Ung H, Brown JE, Johnson KA, Younger J, Hush J, Mackey S. Multivariate classification of structural MRI data detects chronic low back pain. Cereb Cortex 2014;24:1037–44.
    1. Upadhyay J, Geber C, Hargreaves R, Birklein F, Borsook D. A critical evaluation of validity and utility of translational imaging in pain and analgesia: utilizing functional imaging to enhance the process. Neurosci Biobehav Rev 2018;84:407–23.
    1. Vachon-Presseau E, Berger SE, Abdullah TB, Huang L, Cecchi GA, Griffith JW, Schnitzer TJ, Apkarian AV. Brain and psychological determinants of placebo pill response in chronic pain patients. Nat Commun 2018;9:3397.
    1. Vanneste S, Song JJ, De Ridder D. Thalamocortical dysrhythmia detected by machine learning. Nat Commun 2018;9:1103.
    1. Varoquaux G. Cross-validation failure: small sample sizes lead to large error bars. Neuroimage 2018;180:68–77.
    1. Vijayakumar V, Case M, Shirinpour S, He B. Quantifying and characterizing tonic thermal pain across subjects from EEG data using random forest models. IEEE Trans Biomed Eng 2017;64:2988–96.
    1. Vuckovic A, Jose V, Gallardo F, Jarjees M, Fraser M, Purcell M. Prediction of central neuropathic pain in spinal cord injury based on EEG classifier. Clin Neurophysiol 2018;129:1605–17.
    1. Wager TD, Atlas LY, Leotti LA, Rilling JK. Predicting individual differences in placebo analgesia: contributions of brain activity during anticipation and pain experience. J Neurosci 2011;31:439–52.
    1. Wager TD, Atlas LY, Lindquist MA, Roy M, Woo CW, Kross E. An fMRI-based neurologic signature of physical pain. N Engl J Med 2013;368:1388–97.
    1. Walker SM, Beggs S, Baccei ML. Persistent changes in peripheral and spinal nociceptive processing after early tissue injury. Exp Neurol 2016;275:253–60.
    1. Wang X, Baeken C, Fang M, Qiu J, Chen H, Wu GR. Predicting trait-like individual differences in fear of pain in the healthy state using gray matter volume. Brain Imaging Behav 2018:1–6.
    1. Wiech K, Ploner M, Tracey I. Neurocognitive aspects of pain perception. Trends Cogn Sci 2008;12:306–13.
    1. Woo CW, Wager TD. Neuroimaging-based biomarker discovery and validation. PAIN 2015;156:1379–81.
    1. Woo CW, Wager TD. What reliability can and cannot tell us about pain report and pain neuroimaging. PAIN 2016;157:511–13.
    1. Woo CW, Chang LJ, Lindquist MA, Wager TD. Building better biomarkers: brain models in translational neuroimaging. Nat Neurosci 2017;20:365–77.
    1. Woo CW, Koban L, Kross E, Lindquist MA, Banich MT, Ruzic L, Andrews-Hanna JR, Wager TD. Separate neural representations for physical pain and social rejection. Nat Commun 2014;5:1–12.
    1. Woo CW, Roy M, Buhle JT, Wager TD. Distinct brain systems mediate the effects of nociceptive input and self-regulation on pain. PLoS Biol 2015;13:e1002036.
    1. Woo CW, Schmidt L, Krishnan A, Jepma M, Roy M, Lindquist MA, Atlas LY, Wager TD. Quantifying cerebral contributions to pain beyond nociception. Nat Commun 2017;8:1–14.
    1. Younger J, McCue R, Mackey S. Pain outcomes: a brief review of instruments and techniques. Curr Pain Headache Rep 2009;13:39–43.
    1. Zang Y, Jiang T, Lu Y, He Y, Tian L. Regional homogeneity approach to fMRI data analysis. Neuroimage 2004;22:394–400.
    1. Zhang Q, Wu Q, Zhang J, He L, Huang J, Zhang J, Huang H, Gong Q. Discriminative analysis of migraine without aura: using functional and structural MRI with a multi-feature classification approach. PLoS One 2016;11:e0163875.
    1. Zhang Y, Mao Z, Cui Z, Ling Z, Pan L, Liu X, Zhang J, Yu X. Diffusion tensor imaging of axonal and myelin changes in classical trigeminal neuralgia. World Neurosurg 2018;112:e597–607.
    1. Zhong J, Chen DQ, Hung PS, Hayes DJ, Liang KE, Davis KD, Hodaie M. Multivariate pattern classification of brain white matter connectivity predicts classic trigmenial neuralgia. PAIN 2018;159:2076–87.
    1. Zunhammer M, Bingel U, Wager TD. Placebo effects on the neurologic pain signature: a meta-analysis of individual participant functional magnetic resonance imaging data. JAMA Neurol 2018;75:1321–30.

Source: PubMed

3
订阅