Skip to main content

Advertisement

Log in

From the neuromatrix to the pain matrix (and back)

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Pain is a conscious experience, crucial for survival. To investigate the neural basis of pain perception in humans, a large number of investigators apply noxious stimuli to the body of volunteers while sampling brain activity using different functional neuroimaging techniques. These responses have been shown to originate from an extensive network of brain regions, which has been christened the Pain Matrix and is often considered to represent a unique cerebral signature for pain perception. As a consequence, the Pain Matrix is often used to understand the neural mechanisms of pain in health and disease. Because the interpretation of a great number of experimental studies relies on the assumption that the brain responses elicited by nociceptive stimuli reflect the activity of a cortical network that is at least partially specific for pain, it appears crucial to ascertain whether this notion is supported by unequivocal experimental evidence. Here, we will review the original concept of the “Neuromatrix” as it was initially proposed by Melzack and its subsequent transformation into a pain-specific matrix. Through a critical discussion of the evidence in favor and against this concept of pain specificity, we show that the fraction of the neuronal activity measured using currently available macroscopic functional neuroimaging techniques (e.g., EEG, MEG, fMRI, PET) in response to transient nociceptive stimulation is likely to be largely unspecific for nociception.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Notes

  1. Craig et al. (2000) proposed that the posterior insula may constitute a primary “thermosensory cortex”. However, this claim is based mainly on the finding that the magnitude of the responses elicited in this area correlates linearly with the intensity of the noxious stimulus. As shown in the next section, the observation of such a correlation could be satisfactorily explained by the fact that stimuli of greater intensity are also more salient.

References

  • Albe-Fessard D, Berkley KJ, Kruger L, Ralston HJ 3rd, Willis WD Jr (1985) Diencephalic mechanisms of pain sensation. Brain Res 356:217–296

    CAS  PubMed  Google Scholar 

  • Andersson SA, Rydenhag B (1985) Cortical nociceptive systems. Philos Trans R Soc Lond B Biol Sci 308:347–359

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Arendt-Nielsen L (1994) Characteristics, detection, and modulation of laser-evoked vertex potentials. Acta Anaesthesiol Scand Suppl 101:7–44

    CAS  PubMed  Google Scholar 

  • Avenanti A, Bueti D, Galati G, Aglioti SM (2005) Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8:955–960

    CAS  PubMed  Google Scholar 

  • Bancaud J, Talairach J, Geier S, Bonis A, Trottier S, Manrique M (1976) Behavioral manifestations induced by electric stimulation of the anterior cingulate gyrus in man. Rev Neurol (Paris) 132:705–724

    CAS  Google Scholar 

  • Beckmann CF, Smith SA (2004) Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23:137–152

    PubMed  Google Scholar 

  • Beydoun A, Morrow TJ, Shen JF, Casey KL (1993) Variability of laser-evoked potentials: attention, arousal and lateralized differences. Electroencephalogr Clin Neurophysiol 88:173–181

    CAS  PubMed  Google Scholar 

  • Boly M, Faymonville ME, Schnakers C, Peigneux P, Lambermont B, Phillips C, Lancellotti P, Luxen A, Lamy M, Moonen G, Maquet P, Laureys S (2008) Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 7:1013–1020

    PubMed  Google Scholar 

  • Bornhovd K, Quante M, Glauche V, Bromm B, Weiller C, Buchel C (2002) Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. Brain 125:1326–1336

    CAS  PubMed  Google Scholar 

  • Bromm B, Treede RD (1987) Human cerebral potentials evoked by CO2 laser stimuli causing pain. Exp Brain Res 67:153–162

    CAS  PubMed  Google Scholar 

  • Brooks J, Tracey I (2005) From nociception to pain perception: imaging the spinal and supraspinal pathways. J Anat 207:19–33

    PubMed  Google Scholar 

  • Buchel C, Bornhovd K, Quante M, Glauche V, Bromm B, Weiller C (2002) Dissociable neural responses related to pain intensity, stimulus intensity, and stimulus awareness within the anterior cingulate cortex: a parametric single-trial laser functional magnetic resonance imaging study. J Neurosci 22:970–976

    CAS  PubMed  Google Scholar 

  • Budd TW, Michie PT (1994) Facilitation of the N1 peak of the auditory ERP at short stimulus intervals. Neuroreport 5:2513–2516

    CAS  PubMed  Google Scholar 

  • Bushnell MC, Apkarian AV (2005) Representation of pain in the brain. In: McMahon S, Koltzenburg M (eds) Textbook of pain, 5th edn. Churchill Livingstone, Philadelphia, pp 267–289

    Google Scholar 

  • Carmon A, Mor J, Goldberg J (1976) Evoked cerebral responses to noxious thermal stimuli in humans. Exp Brain Res 25:103–107

    CAS  PubMed  Google Scholar 

  • Carmon A, Dotan Y, Sarne Y (1978) Correlation of subjective pain experience with cerebral evoked responses to noxious thermal stimulations. Exp Brain Res 33:445–453

    CAS  PubMed  Google Scholar 

  • Chapman CR, Chen AC, Colpitts YM, Martin RW (1981a) Sensory decision theory describes evoked potentials in pain discrimination. Psychophysiology 18:114–120

    CAS  PubMed  Google Scholar 

  • Chapman CR, Colpitts YH, Mayeno JK, Gagliardi GJ (1981b) Rate of stimulus repetition changes evoked potential amplitude: dental and auditory modalities compared. Exp Brain Res 43:246–252

    CAS  PubMed  Google Scholar 

  • Charlesworth G, Soryal I, Smith S, Sisodiya SM (2009) Acute, localised paroxysmal pain as the initial manifestation of focal seizures: a case report and a brief review of the literature. Pain 141:300–305

    PubMed  Google Scholar 

  • Cheng Y, Lin CP, Liu HL, Hsu YY, Lim KE, Hung D, Decety J (2007) Expertise modulates the perception of pain in others. Curr Biol 17:1708–1713

    CAS  PubMed  Google Scholar 

  • Clark JA, Brown CA, Jones AK, El-Deredy W (2008) Dissociating nociceptive modulation by the duration of pain anticipation from unpredictability in the timing of pain. Clin Neurophysiol 119:2870–2878

    Google Scholar 

  • Coghill RC, Sang CN, Maisog JM, Iadarola MJ (1999) Pain intensity processing within the human brain: a bilateral, distributed mechanism. J Neurophysiol 82:1934–1943

    CAS  PubMed  Google Scholar 

  • Corkin S, Hebben N (1981) Subjective estimates of chronic pain before and after psychosurgery or treatment in a pain unit. Pain 1:S150

    Google Scholar 

  • Craig AD (2003) Pain mechanisms: labeled lines versus convergence in central processing. Annu Rev Neurosci 26:1–30

    CAS  PubMed  Google Scholar 

  • Craig AD, Bushnell MC, Zhang ET, Blomqvist A (1994) A thalamic nucleus specific for pain and temperature sensation. Nature 372:770–773

    CAS  PubMed  Google Scholar 

  • Craig AD, Chen K, Bandy D, Reiman EM (2000) Thermosensory activation of insular cortex. Nat Neurosci 3:184–190

    CAS  PubMed  Google Scholar 

  • Derbyshire SW, Jones AK, Gyulai F, Clark S, Townsend D, Firestone LL (1997) Pain processing during three levels of noxious stimulation produces differential patterns of central activity. Pain 73:431–445

    CAS  PubMed  Google Scholar 

  • Descartes R (1649) Les passions de l’âme. L. Elzevir, Amsterdam

    Google Scholar 

  • Dillmann J, Miltner WH, Weiss T (2000) The influence of semantic priming on event-related potentials to painful laser-heat stimuli in humans. Neurosci Lett 284:53–56

    CAS  PubMed  Google Scholar 

  • Dong WK, Chudler EH, Sugiyama K, Roberts VJ, Hayashi T (1994) Somatosensory, multisensory, and task-related neurons in cortical area 7b (PF) of unanesthetized monkeys. J Neurophysiol 72:542–564

    CAS  PubMed  Google Scholar 

  • Downar J, Crawley AP, Mikulis DJ, Davis KD (2000) A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci 3:277–283

    CAS  PubMed  Google Scholar 

  • Downar J, Mikulis DJ, Davis KD (2003) Neural correlates of the prolonged salience of painful stimulation. Neuroimage 20:1540–1551

    PubMed  Google Scholar 

  • Dum RP, Levinthal DJ, Strick PL (2009) The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. J Neurosci 29:14223–14235

    CAS  PubMed  Google Scholar 

  • Eisenberger NI, Lieberman MD, Williams KD (2003) Does rejection hurt? An FMRI study of social exclusion. Science 302:290–292

    CAS  PubMed  Google Scholar 

  • Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10:382–390

    PubMed  Google Scholar 

  • Foltz EL, White LE Jr (1962) Pain “relief” by frontal cingulumotomy. J Neurosurg 19:89–100

    CAS  PubMed  Google Scholar 

  • Foltz EL, White LE (1968) The role of rostral cingulumotomy in “pain” relief. Int J Neurol 6:353–373

    CAS  PubMed  Google Scholar 

  • Frot M, Magnin M, Mauguiere F, Garcia-Larrea L (2007) Human SII and posterior insula differently encode thermal laser stimuli. Cereb Cortex 17:610–620

    PubMed  Google Scholar 

  • Frot M, Mauguiere F, Magnin M, Garcia-Larrea L (2008) Parallel processing of nociceptive A-delta inputs in SII and midcingulate cortex in humans. J Neurosci 28:944–952

    CAS  PubMed  Google Scholar 

  • Garcia-Larrea L, Peyron R, Laurent B, Mauguiere F (1997) Association and dissociation between laser-evoked potentials and pain perception. Neuroreport 8:3785–3789

    CAS  PubMed  Google Scholar 

  • Garcia-Larrea L, Convers P, Magnin M, Andre-Obadia N, Peyron R, Laurent B, Mauguiere F (2002) Laser-evoked potential abnormalities in central pain patients: the influence of spontaneous and provoked pain. Brain 125:2766–2781

    PubMed  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

    CAS  PubMed  Google Scholar 

  • Godinho F, Magnin M, Frot M, Perchet C, Garcia-Larrea L (2006) Emotional modulation of pain: is it the sensation or what we recall? J Neurosci 26:11454–11461

    CAS  PubMed  Google Scholar 

  • Gracely RH, Geisser ME, Giesecke T, Grant MA, Petzke F, Williams DA, Clauw DJ (2004) Pain catastrophizing and neural responses to pain among persons with fibromyalgia. Brain 127:835–843

    CAS  PubMed  Google Scholar 

  • Greenspan JD, Winfield JA (1992) Reversible pain and tactile deficits associated with a cerebral tumor compressing the posterior insula and parietal operculum. Pain 50:29–39

    CAS  PubMed  Google Scholar 

  • Greenspan JD, Lee RR, Lenz FA (1999) Pain sensitivity alterations as a function of lesion location in the parasylvian cortex. Pain 81:273–282

    CAS  PubMed  Google Scholar 

  • Head H, Holmes G (1911) Sensory disturbances from cerebral lesions. Brain 34:102–254

    Google Scholar 

  • Hofbauer RK, Rainville P, Duncan GH, Bushnell MC (2001) Cortical representation of the sensory dimension of pain. J Neurophysiol 86:402–411

    CAS  PubMed  Google Scholar 

  • Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195:215–243

    CAS  PubMed  Google Scholar 

  • Hurt RW, Ballantine HT Jr (1973) Stereotactic anterior cingulate lesions for persistent pain: a report on 68 cases. Clin Neurosurg 21:334–351

    Google Scholar 

  • Hutchison WD, Davis KD, Lozano AM, Tasker RR, Dostrovsky JO (1999) Pain-related neurons in the human cingulate cortex. Nat Neurosci 2:403–405

    CAS  PubMed  Google Scholar 

  • Iannetti GD, Zambreanu L, Cruccu G, Tracey I (2005) Operculoinsular cortex encodes pain intensity at the earliest stages of cortical processing as indicated by amplitude of laser-evoked potentials in humans. Neuroscience 131:199–208

    CAS  PubMed  Google Scholar 

  • Iannetti GD, Hughes NP, Lee MC, Mouraux A (2008) Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? J Neurophysiol 100:815–828

    CAS  PubMed  Google Scholar 

  • Iannetti GD, Lee MC, Mouraux A (2010) A multisensory investigation of the functional significance of the “pain matrix”. 13th World Congress on Pain, Montreal, Canada

  • Imig TJ, Adrian HO (1977) Binaural columns in the primary field (A1) of cat auditory cortex. Brain Res 138:241–257

    CAS  PubMed  Google Scholar 

  • Ingvar M (1999) Pain and functional imaging. Philos Trans R Soc Lond B Biol Sci 354:1347–1358

    CAS  PubMed  Google Scholar 

  • Ingvar M, Hsieg J-C (1999) The image of pain. In: Wall PD, Melzack R (eds) The textbook of pain, 4th edn. Churchill Livingstone, Edinburgh

    Google Scholar 

  • Isnard J, Guenot M, Ostrowsky K, Sindou M, Mauguiere F (2000) The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 48:614–623

    CAS  PubMed  Google Scholar 

  • Isnard J, Guenot M, Sindou M, Mauguiere F (2004) Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 45:1079–1090

    PubMed  Google Scholar 

  • Itti L, Koch C (2001) Computational modelling of visual attention. Nat Rev Neurosci 2:194–203

    CAS  PubMed  Google Scholar 

  • Jackson PL, Meltzoff AN, Decety J (2005) How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 24:771–779

    PubMed  Google Scholar 

  • Jones A (1998a) The pain matrix and neuropathic pain. Brain 121(Pt 5):783–784

    PubMed  Google Scholar 

  • Jones EG (1998b) Viewpoint: the core and matrix of thalamic organization. Neuroscience 85:331–345

    CAS  PubMed  Google Scholar 

  • Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Philos Trans R Soc Lond B Biol Sci 357:1659–1673

    PubMed  Google Scholar 

  • Kaas JH, Collins CE (2001) The organization of sensory cortex. Curr Opin Neurobiol 11:498–504

    CAS  PubMed  Google Scholar 

  • Kakigi R, Shibasaki H (1992) Mechanisms of pain relief by vibration and movement. J Neurol Neurosurg Psychiatry 55:282–286

    CAS  PubMed  Google Scholar 

  • Kakigi R, Inui K, Tran DT, Qiu Y, Wang X, Watanabe S, Hoshiyama M (2004) Human brain processing and central mechanisms of pain as observed by electro- and magneto-encephalography. J Chin Med Assoc 67:377–386

    PubMed  Google Scholar 

  • Kandel E, Schwartz J, Jessel T (2000) Principles of neural science. McGraw, Hill

    Google Scholar 

  • Kayser C, Petkov CI, Lippert M, Logothetis NK (2005) Mechanisms for allocating auditory attention: an auditory saliency map. Curr Biol 15:1943–1947

    CAS  PubMed  Google Scholar 

  • Kenshalo DR, Douglass DK (1995) The role of the cerebral cortex in the experience of pain. In: Bromm B, Desmedt JE (eds) Pain and the brain: from nociception to cognition. Raven Press, New York, pp 21–34

    Google Scholar 

  • Kenshalo DR Jr, Isensee O (1983) Responses of primate SI cortical neurons to noxious stimuli. J Neurophysiol 50:1479–1496

    PubMed  Google Scholar 

  • Kenshalo DR, Iwata K, Sholas M, Thomas DA (2000) Response properties and organization of nociceptive neurons in area 1 of monkey primary somatosensory cortex. J Neurophysiol 84:719–729

    CAS  PubMed  Google Scholar 

  • Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 30:57–78

    CAS  PubMed  Google Scholar 

  • Kunde V, Treede RD (1993) Topography of middle-latency somatosensory evoked potentials following painful laser stimuli and non-painful electrical stimuli. Electroencephalogr Clin Neurophysiol 88:280–289

    CAS  PubMed  Google Scholar 

  • Kwong KK, Belliveau JW, Chesler DA, Goldberg IE, Weisskoff RM, Poncelet BP, Kennedy DN, Hoppel BE, Cohen MS, Turner R et al (1992) Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 89:5675–5679

    CAS  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

    CAS  PubMed  Google Scholar 

  • Legrain V, Guerit JM, Bruyer R, Plaghki L (2002) Attentional modulation of the nociceptive processing into the human brain: selective spatial attention, probability of stimulus occurrence, and target detection effects on laser evoked potentials. Pain 99:21–39

    PubMed  Google Scholar 

  • Legrain V, Guerit JM, Bruyer R, Plaghki L (2003) Electrophysiological correlates of attentional orientation in humans to strong intensity deviant nociceptive stimuli, inside and outside the focus of spatial attention. Neurosci Lett 339:107–110

    CAS  PubMed  Google Scholar 

  • Legrain V, Damme SV, Eccleston C, Davis KD, Seminowicz DA, Crombez G (2009a) A neurocognitive model of attention to pain: behavioral and neuroimaging evidence. Pain 144:230–232

    PubMed  Google Scholar 

  • Legrain V, Perchet C, Garcia-Larrea L (2009b) Involuntary orienting of attention to nociceptive events: neural and behavioral signatures. J Neurophysiol 102:2423–2434

    PubMed  Google Scholar 

  • Logothetis NK (2008) What we can do and what we cannot do with fMRI. Nature 453:869–878

    CAS  PubMed  Google Scholar 

  • Loveless N, Hari R, Hamalainen M, Tiihonen J (1989) Evoked responses of human auditory cortex may be enhanced by preceding stimuli. Electroencephalogr Clin Neurophysiol 74:217–227

    CAS  PubMed  Google Scholar 

  • Lui F, Duzzi D, Corradini M, Serafini M, Baraldi P, Porro CA (2008) Touch or pain? Spatio-temporal patterns of cortical fMRI activity following brief mechanical stimuli. Pain 138:362–374

    CAS  PubMed  Google Scholar 

  • Mauguiere F, Courjon J (1978) Somatosensory epilepsy. A review of 127 cases. Brain 101:307–332

    CAS  PubMed  Google Scholar 

  • Melzack R (1989) Phantom limbs, the self and the brain. Can Psychol 30:1–16

    Google Scholar 

  • Melzack R (2005) Evolution of the neuromatrix theory of pain. The Prithvi Raj Lecture: presented at the third World Congress of World Institute of Pain, Barcelona 2004. Pain Pract 5:85–94

    PubMed  Google Scholar 

  • Mesulam MM (1998) From sensation to cognition. Brain 121(Pt 6):1013–1052

    PubMed  Google Scholar 

  • Miller G (2009) Neuroscience. Brain scans of pain raise questions for the law. Science 323:195

    CAS  PubMed  Google Scholar 

  • Moisset X, Bouhassira D (2007) Brain imaging of neuropathic pain. Neuroimage 37(1):S80–S88

    PubMed  Google Scholar 

  • Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434

    CAS  PubMed  Google Scholar 

  • Mountcastle VB, Davies PW, Berman AL (1957) Response properties of neurons of cat’s somatic sensory cortex to peripheral stimuli. J Neurophysiol 20:374–407

    CAS  PubMed  Google Scholar 

  • Mouraux A, Iannetti GD (2008) A review of the evidence against the “first come first served” hypothesis. Comment on Truini et al. [Pain 2007; 131:43–47]. Pain 136:219–221; author reply 222–213

  • Mouraux A, Iannetti GD (2009) Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J Neurophysiol 101:3258–3269

    CAS  PubMed  Google Scholar 

  • Mouraux A, Plaghki L (2007) Cortical interactions and integration of nociceptive and non-nociceptive somatosensory inputs in humans. Neuroscience 150:72–81

    CAS  PubMed  Google Scholar 

  • Mouraux A, Guerit JM, Plaghki L (2003) Non-phase locked electroencephalogram (EEG) responses to CO2 laser skin stimulations may reflect central interactions between Aδ- and C-fibre afferent volleys. Clin Neurophysiol 114:710–722

    CAS  PubMed  Google Scholar 

  • Mouraux A, Guerit JM, Plaghki L (2004) Refractoriness cannot explain why C-fiber laser-evoked brain potentials are recorded only if concomitant Adelta-fiber activation is avoided. Pain 112:16–26

    CAS  PubMed  Google Scholar 

  • Naatanen R, Picton T (1987) The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24:375–425

    CAS  PubMed  Google Scholar 

  • Naatanen R, Paavilainen P, Rinne T, Alho K (2007) The mismatch negativity (MMN) in basic research of central auditory processing: a review. Clin Neurophysiol 118:2544–2590

    CAS  PubMed  Google Scholar 

  • Nahra H, Plaghki L (2003) Modulation of perception and neurophysiological correlates of brief CO2 laser stimuli in humans using concurrent large fiber stimulation. Somatosens Mot Res 20:139–147

    PubMed  Google Scholar 

  • Ohara S, Crone NE, Weiss N, Treede RD, Lenz FA (2004) Amplitudes of laser evoked potential recorded from primary somatosensory, parasylvian and medial frontal cortex are graded with stimulus intensity. Pain 110:318–328

    CAS  PubMed  Google Scholar 

  • Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguiere F (2002) Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cereb Cortex 12:376–385

    PubMed  Google Scholar 

  • Plaghki L, Delisle D, Godfraind JM (1994) Heterotopic nociceptive conditioning stimuli and mental task modulate differently the perception and physiological correlates of short CO2 laser stimuli. Pain 57:181–192

    CAS  PubMed  Google Scholar 

  • Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, Rawlins JN (1999) Dissociating pain from its anticipation in the human brain. Science 284:1979–1981

    CAS  PubMed  Google Scholar 

  • Ploner M, Gross J, Timmermann L, Schnitzler A (2002) Cortical representation of first and second pain sensation in humans. Proc Natl Acad Sci USA 99:12444–12448

    CAS  PubMed  Google Scholar 

  • Porro CA (2003) Functional imaging and pain: behavior, perception, and modulation. Neuroscientist 9:354–369

    PubMed  Google Scholar 

  • Porro CA, Cettolo V, Francescato MP, Baraldi P (1998) Temporal and intensity coding of pain in human cortex. J Neurophysiol 80:3312–3320

    CAS  PubMed  Google Scholar 

  • Raij TT, Vartiainen NV, Jousmaki V, Hari R (2003) Effects of interstimulus interval on cortical responses to painful laser stimulation. J Clin Neurophysiol 20:73–79

    PubMed  Google Scholar 

  • Rainville P (2002) Brain mechanisms of pain affect and pain modulation. Curr Opin Neurobiol 12:195–204

    CAS  PubMed  Google Scholar 

  • Rainville P, Duncan GH, Price DD, Carrier B, Bushnell MC (1997) Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277:968–971

    CAS  PubMed  Google Scholar 

  • Robinson CJ, Burton H (1980) Somatotopographic organization in the second somatosensory area of M. fascicularis. J Comp Neurol 192:43–67

    CAS  PubMed  Google Scholar 

  • Schnitzler A, Ploner M (2000) Neurophysiology and functional neuroanatomy of pain perception. J Clin Neurophysiol 17:592–603

    CAS  PubMed  Google Scholar 

  • Schweinhardt P, Bountra C, Tracey I (2006) Pharmacological FMRI in the development of new analgesic compounds. NMR Biomed 19:702–711

    CAS  PubMed  Google Scholar 

  • 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 27:2349–2356

    CAS  PubMed  Google Scholar 

  • Sikes RW, Vogt BA (1992) Nociceptive neurons in area 24 of rabbit cingulate cortex. J Neurophysiol 68:1720–1732

    CAS  PubMed  Google Scholar 

  • Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303:1157–1162

    CAS  PubMed  Google Scholar 

  • Sokolov EN (1975) The neuronal mechanisms of the orienting reflex. In: Sokolov EN, Vinogradova OS (eds) The neuronal mechanisms of the orienting reflex. Lawrence Erlbaum Associates, Hillsdale, pp 217–235

    Google Scholar 

  • Speckmann E, Elger C (1999) Introduction to the neurophysiological basis of the EEG and DC potentials. In: Niedermeyer E, Lopes Da Silva F (eds) Electroencephalography. Basic principles, clinical applications, and related fields. Lippincott Williams and Wilkins, Baltimore, pp 15–27

    Google Scholar 

  • Starr CJ, Sawaki L, Wittenberg GF, Burdette JH, Oshiro Y, Quevedo AS, Coghill RC (2009) Roles of the insular cortex in the modulation of pain: insights from brain lesions. J Neurosci 29:2684–2694

    CAS  PubMed  Google Scholar 

  • Stern J, Jeanmonod D, Sarnthein J (2006) Persistent EEG overactivation in the cortical pain matrix of neurogenic pain patients. Neuroimage 31:721–731

    PubMed  Google Scholar 

  • Stowell H (1984) Event related brain potentials and human pain: a first objective overview. Int J Psychophysiol 1:137–151

    CAS  PubMed  Google Scholar 

  • Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH (1991) Multiple representations of pain in human cerebral cortex. Science 251:1355–1358

    CAS  PubMed  Google Scholar 

  • 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 86:1499–1503

    CAS  PubMed  Google Scholar 

  • Tolle TR, Kaufmann T, Siessmeier T, Lautenbacher S, Berthele A, Munz F, Zieglgansberger W, Willoch F, Schwaiger M, Conrad B, Bartenstein P (1999) Region-specific encoding of sensory and affective components of pain in the human brain: a positron emission tomography correlation analysis. Ann Neurol 45:40–47

    CAS  PubMed  Google Scholar 

  • Tracey I (2005) Nociceptive processing in the human brain. Curr Opin Neurobiol 15:478–487

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Treede RD (2006) Chapter 1 pain and hyperalgesia: definitions and theories. Handb Clin Neurol 81:3–10

    PubMed  Google Scholar 

  • Treede RD, Kenshalo DR, Gracely RH, Jones AK (1999) The cortical representation of pain. Pain 79:105–111

    CAS  PubMed  Google Scholar 

  • Truini A, Rossi P, Galeotti F, Romaniello A, Virtuoso M, De Lena C, Leandri M, Cruccu G (2004) Excitability of the Adelta nociceptive pathways as assessed by the recovery cycle of laser evoked potentials in humans. Exp Brain Res 155:120–123

    CAS  PubMed  Google Scholar 

  • Truini A, Galeotti F, Cruccu G, Garcia-Larrea L (2007) Inhibition of cortical responses to Adelta inputs by a preceding C-related response: testing the “first come, first served” hypothesis of cortical laser evoked potentials. Pain 131:341–347

    CAS  PubMed  Google Scholar 

  • Valeriani M, Betti V, Le Pera D, De Armas L, Miliucci R, Restuccia D, Avenanti A, Aglioti SM (2008) Seeing the pain of others while being in pain: a laser-evoked potentials study. Neuroimage 40:1419–1428

    PubMed  Google Scholar 

  • Van Damme S, Legrain V, Vogt J, Crombez G (2010) Keeping pain in mind: a motivational account of attention to pain. Neurosci Biobehav Rev 34:204–213

    PubMed  Google Scholar 

  • Wall PD (1995) Independent mechanisms converge on pain. Nat Med 1:740–741

    CAS  PubMed  Google Scholar 

  • Wang AL, Mouraux A, Liang M, Iannetti GD (2008) The enhancement of the N1 wave elicited by sensory stimuli presented at very short inter-stimulus intervals is a general feature across sensory systems. PLoS ONE 3:e3929

    PubMed  Google Scholar 

  • Wang AL, Mouraux A, Meng L, Iannetti GD (in press) Stimulus novelty and not neural refractoriness explains the repetition suppression of laser-evoked potentials (LEPs). J Neurophysiol

  • Whitsel BL, Petrucelli LM, Werner G (1969) Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. J Neurophysiol 32:170–183

    CAS  PubMed  Google Scholar 

  • Whitsel BL, Favorov OV, Li Y, Quibrera M, Tommerdahl M (2009) Area 3a neuron response to skin nociceptor afferent drive. Cereb Cortex 19:349–366

    PubMed  Google Scholar 

  • Whyte J (2008) Clinical implications of the integrity of the pain matrix. Lancet Neurol 7:979–980

    PubMed  Google Scholar 

  • Yamamura H, Iwata K, Tsuboi Y, Toda K, Kitajima K, Shimizu N, Nomura H, Hibiya J, Fujita S, Sumino R (1996) Morphological and electrophysiological properties of ACCx nociceptive neurons in rats. Brain Res 735:83–92

    CAS  PubMed  Google Scholar 

  • Yantis S (2008) The neural basis of selective attention: cortical sources and targets of attentional modulation. Curr Dir Psychol Sci 17:86–90

    PubMed  Google Scholar 

  • Young GB, Blume WT (1983) Painful epileptic seizures. Brain 106(Pt 3):537–554

    PubMed  Google Scholar 

Download references

Acknowledgments

AM is supported by the Belgian National Fund for Scientific Research (FNRS) and has received funding from the EFIC Grünenthal grant. GDI is University Research Fellow of The Royal Society and acknowledges the support of the BBSRC. The authors are grateful to the members of the GAMFI Centre for useful discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. D. Iannetti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iannetti, G.D., Mouraux, A. From the neuromatrix to the pain matrix (and back). Exp Brain Res 205, 1–12 (2010). https://doi.org/10.1007/s00221-010-2340-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-010-2340-1

Keywords

Navigation