Crossmodal shaping of pain: A multisensory approach to nociception

Trends in Cognitive Sciences

Volumn 18, Issue 6, 2014, Pages 319-327

  Senkowski, Daniel ^a   Höfle, Marion ^b   Engel, Andreas K ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

Attention network; Functional connectivity; Multisensory processing; Oscillatory activity; Pain processing; Salience network

Indexed keywords

SENSORY PERCEPTION;

CROSS-MODAL; FUNCTIONAL CONNECTIVITY; MULTISENSORY; NEURAL MECHANISMS; NOCICEPTION; RESEARCH FIELDS; SENSORY MODALITY;

HEALTH;

ATTENTION; CORTICAL SYNCHRONIZATION; DELTA RHYTHM; EMOTION; FACIAL EXPRESSION; HUMAN; LIMB PROSTHESIS; NEUROMODULATION; NOCICEPTION; NOCICEPTIVE STIMULATION; REVIEW; STIMULUS RESPONSE; VIRTUAL REALITY; VISUAL STIMULATION; BIOLOGICAL MODEL; BRAIN; NERVE TRACT; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY;

ATTENTION; BRAIN; HUMANS; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NOCICEPTION; PAIN; PAIN PERCEPTION;

EID: 84901395204     PISSN: 13646613     EISSN: 1879307X     Source Type: Journal    
DOI: 10.1016/j.tics.2014.03.005     Document Type: Review

References (95)

1. Donaldson G.W., et al. Pain and the defense response: structural equation modeling reveals a coordinated psychophysiological response to increasing painful stimulation. Pain 2003, 102:97-108.
2. Legrain V., et al. The pain matrix reloaded: a salience detection system for the body. Prog. Neurobiol. 2011, 93:111-124.
3. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
4. Iannetti G.D., Mouraux A. From the neuromatrix to the pain matrix (and back). Exp. Brain Res. 2010, 205:1-12.
5. Kulkarni B., et al. Attention to pain localization and unpleasantness discriminates the functions of the medial and lateral pain systems. Eur. J. Neurosci. 2005, 21:3133-3142.
6. Hauck M., et al. Attention to painful stimulation enhances gamma-band activity and synchronization in human sensorimotor cortex. J. Neurosci. 2007, 27:9270-9277.
7. Legrain V., et al. Involuntary orientation of attention to unattended deviant nociceptive stimuli is modulated by concomitant visual task difficulty. Evidence from laser evoked potentials. Clin. Neurophysiol. 2005, 116:2165-2174.
8. Spence C., et al. Selective attention to pain: a psychophysical investigation. Exp. Brain Res. 2002, 145:395-402.
9. Zampini M., et al. 'Prior entry' for pain: attention speeds the perceptual processing of painful stimuli. Neurosci. Lett. 2007, 414:75-79.
10. Talsma D., et al. The multifaceted interplay between attention and multisensory integration. Trends Cogn. Sci. 2010, 14:400-410.
11. Pomper U., et al. Crossmodal bias of visual input on pain perception and pain-induced beta activity. Neuroimage 2013, 66:469-478.
12. Hauck M., et al. The influence of music and music therapy on pain-induced neuronal oscillations measured by magnetencephalography. Pain 2013, 154:539-547.
13. Godinho F., et al. Pain influences hedonic assessment of visual inputs. Eur. J. Neurosci. 2008, 27:2219-2228.
14. Longo M.R., et al. Visually induced analgesia: seeing the body reduces pain. J. Neurosci. 2009, 29:12125-12130.
15. Hipp J.F., et al. Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat. Neurosci. 2012, 15:884-890.
16. Schneider T.R., et al. Gamma-band activity as a signature for cross-modal priming of auditory object recognition by active haptic exploration. J. Neurosci. 2011, 31:2502-2510.
17. Schepers I.M., et al. Noise alters beta-band activity in superior temporal cortex during audiovisual speech processing. Neuroimage 2013, 70:101-112.
18. Lakatos P., et al. Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 2007, 53:279-292.
19. Kayser C., Logothetis N.K. Directed interactions between auditory and superior temporal cortices and their role in sensory integration. Front. Integr. Neurosci. 2009, 3:7.
20. Senkowski D., et al. Crossmodal binding through neural coherence: implications for multisensory processing. Trends Neurosci. 2008, 31:401-409.
21. Senkowski D., et al. Emotional facial expressions modulate pain-induced beta and gamma oscillations in sensorimotor cortex. J. Neurosci. 2011, 31:14542-14550.
22. Mancini F., et al. Changes in cortical oscillations linked to multisensory modulation of nociception. Eur. J. Neurosci. 2012, 37:768-776.
23. Haggard P., et al. Spatial sensory organization and body representation in pain perception. Curr. Biol. 2013, 23:R164-R176.
24. Stein B.E., Meredith M.A. The Merging of the Senses 1993, MIT Press.
25. Stein B.E., Stanford T.R. Multisensory integration: current issues from the perspective of the single neuron. Nat. Rev. Neurosci. 2008, 9:255-266.
26. Senkowski D., et al. Multisensory processing and oscillatory activity: analyzing non-linear electrophysiological measures in humans and simians. Exp. Brain Res. 2007, 177:184-195.
27. Inui K., et al. Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans. Cereb. Cortex 2006, 16:355-365.
28. Van Ryckeghem D.M., et al. The role of spatial attention in attentional control over pain: an experimental investigation. Exp. Brain Res. 2011, 208:269-275.
29. Rhudy J.L., et al. Habituation, sensitization, and emotional valence modulation of pain responses. Pain 2010, 148:320-327.
30. Roy M., et al. Cerebral and spinal modulation of pain by emotions. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:20900-20905.
31. Stancak A., et al. Modulation of pain by emotional sounds: a laser-evoked potential study. Eur. J. Pain 2013, 17:324-335.
32. Roy M., et al. Emotional valence contributes to music-induced analgesia. Pain 2008, 134:140-147.
33. Villemure C., et al. Effects of odors on pain perception: deciphering the roles of emotion and attention. Pain 2003, 106:101-108.
34. Villemure C., Bushnell M.C. Mood influences supraspinal pain processing separately from attention. J. Neurosci. 2009, 29:705-715.
35. Graziano M.S., Cooke D.F. Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia 2006, 44:845-859.
36. Mohan R., et al. No pain relief with the rubber hand illusion. PLoS ONE 2012, 7:e52400.
37. Martini M., et al. What color is my arm? Changes in skin color of an embodied virtual arm modulates pain threshold. Front. Hum. Neurosci. 2013, 7:438.
38. Höfle M., et al. Viewing a needle pricking a hand that you perceive as yours enhances unpleasantness of pain. Pain 2012, 153:1074-1081.
39. Höfle M., et al. Spectral signatures of viewing a needle approaching one's body when anticipating pain. Eur. J. Neurosci. 2013, 38:3089-3098.
40. Mancini F., et al. Visual distortion of body size modulates pain perception. Psychol. Sci. 2011, 22:325-330.
41. Longo M.R., et al. Linking pain and the body: neural correlates of visually induced analgesia. J. Neurosci. 2012, 32:2601-2607.
42. Ehrsson H.H., et al. Threatening a rubber hand that you feel is yours elicits a cortical anxiety response. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:9828-9833.
43. Ramachandran V.S., et al. Touching the phantom limb. Nature 1995, 377:489-490.
44. Markman T., et al. EEG analysis reveals widespread directed functional interactions related to a painful cutaneous laser stimulus. J. Neurophysiol. 2013, 110:2440-2449.
45. Gross J., et al. Gamma oscillations in human primary somatosensory cortex reflect pain perception. PLoS Biol. 2007, 5:e133.
46. Zhang Z.G., et al. Gamma-band oscillations in the primary somatosensory cortex - a direct and obligatory correlate of subjective pain intensity. J. Neurosci. 2012, 32:7429-7438.
47. Ploner M., et al. Oscillatory activity reflects the excitability of the human somatosensory system. Neuroimage 2006, 32:1231-1236.
48. Tiemann L., et al. Gamma oscillations as a neuronal correlate of the attentional effects of pain. Pain 2010, 150:302-308.
49. Shao S., et al. Frequency-domain EEG source analysis for acute tonic cold pain perception. Clin. Neurophysiol. 2012, 123:2042-2049.
50. Ohara S., et al. Analysis of synchrony demonstrates 'pain networks' defined by rapidly switching, task-specific, functional connectivity between pain-related cortical structures. Pain 2006, 123:244-253.
51. Ploner M., et al. Functional integration within the human pain system as revealed by Granger causality. Hum. Brain Mapp. 2009, 30:4025-4032.
52. Liu C.C., et al. Attention to painful cutaneous laser stimuli evokes directed functional connectivity between activity recorded directly from human pain-related cortical structures. Pain 2011, 152:664-675.
53. Liu C.C., et al. Attention to painful cutaneous laser stimuli evokes directed functional interactions between human sensory and modulatory pain-related cortical areas. Pain 2011, 152:2781-2791.
54. Schoffelen J.M., Gross J. Source connectivity analysis with MEG and EEG. Hum. Brain Mapp. 2009, 30:1857-1865.
55. Siegel M., et al. Spectral fingerprints of large-scale neuronal interactions. Nat. Rev. Neurosci. 2012, 13:121-134.
56. Engel A.K., et al. Multisensory integration through neural coherence. The Neural Bases of Multisensory Processing 2012, 115-130. CRC Press. M.M. Murray, M.T. Wallace (Eds.).
57. Hipp J.F., et al. Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron 2011, 69:387-396.
58. Keil J., et al. On the variability of the McGurk effect: audiovisual integration depends on prestimulus brain states. Cereb. Cortex 2012, 22:221-231.
59. Keil J., et al. Prestimulus beta power and phase synchrony influence the sound-induced flash illusion. Cereb. Cortex 2014, 24:1278-1288.
60. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
61. Frot M., et al. Cortical representation of pain in primary sensory-motor areas (S1/M1) - a study using intracortical recordings in humans. Hum. Brain Mapp. 2013, 34:2655-2668.
62. Frot M., et al. Parallel processing of nociceptive A-delta inputs in SII and midcingulate cortex in humans. J. Neurosci. 2008, 28:944-952.
63. Mouraux A., Iannetti G.D. Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J. Neurophysiol. 2009, 101:3258-3269.
64. Iannetti G.D., et al. Determinants of laser-evoked EEG responses: pain perception or stimulus saliency?. J. Neurophysiol. 2008, 100:815-828.
65. Garcia-Larrea L. The posterior insular-opercular region and the search of a primary cortex for pain. Neurophysiol. Clin. 2012, 42:299-313.
66. Legrain V., et al. Shielding cognition from nociception with working memory. Cortex 2012, 49:1922-1934.
67. Zu Eulenburg P., et al. Interoceptive and multimodal functions of the operculo-insular cortex: tactile, nociceptive and vestibular representations. Neuroimage 2013, 83:75-86.
68. Ploner M., et al. Flexible cerebral connectivity patterns subserve contextual modulations of pain. Cereb. Cortex 2011, 21:719-726.
69. Atlas L.Y., et al. Brain mediators of predictive cue effects on perceived pain. J. Neurosci. 2010, 30:12964-12977.
70. Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 2009, 32:209-224.
71. Ghazanfar A.A., Schroeder C.E. Is neocortex essentially multisensory?. Trends Cogn. Sci. 2006, 10:278-285.
72. Cacchio A., et al. Mirror therapy for chronic complex regional pain syndrome type 1 and stroke. N. Engl. J. Med. 2009, 361:634-636.
73. Chan B.L., et al. Mirror therapy for phantom limb pain. N. Engl. J. Med. 2007, 357:2206-2207.
74. Ramachandran V.S., Hirstein W. The perception of phantom limbs. The D. O. Hebb lecture. Brain 1998, 121:1603-1630.
75. Schmalzl L., et al. An alternative to traditional mirror therapy: illusory touch can reduce phantom pain when illusory movement does not. Clin. J. Pain 2013, 29:e10-e18.
76. Preston C., Newport R. Analgesic effects of multisensory illusions in osteoarthritis. Rheumatology (Oxford) 2011, 50:2314-2315.
77. Spence C., et al. Crossmodal processing. Exp. Brain Res. 2009, 198:107-111.
78. Engel A.K., Fries P. Beta-band oscillations - signalling the status quo?. Curr. Opin. Neurobiol. 2010, 20:156-165.
79. Schulz E., et al. Gamma oscillations are involved in the sensorimotor transformation of pain. J. Neurophysiol. 2012, 108:1025-1031.
80. Jensen O., et al. Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 2007, 30:317-324.
81. Siegel M., et al. Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron 2008, 60:709-719.
82. Ploner M., et al. Pain suppresses spontaneous brain rhythms. Cereb. Cortex 2006, 16:537-540.
83. Raij T.T., et al. Modulation of motor-cortex oscillatory activity by painful Adelta- and C-fiber stimuli. Neuroimage 2004, 23:569-573.
84. Stancak A., et al. EEG source analysis and fMRI reveal two electrical sources in the fronto-parietal operculum during subepidermal finger stimulation. Neuroimage 2005, 25:8-20.
85. Hauck M., et al. Role of synchronized oscillatory brain activity for human pain perception. Rev. Neurosci. 2008, 19:10.
86. Auvray M., et al. The sensory-discriminative and affective-motivational aspects of pain. Neurosci. Biobehav. Rev. 2010, 34:214-223.
87. Treede R.D., et al. The cortical representation of pain. Pain 1999, 79:105-111.
88. Rainville P., et al. Dissociation of sensory and affective dimensions of pain using hypnotic modulation. Pain 1999, 82:159-171.
89. Price D.D. Psychological and neural mechanisms of the affective dimension of pain. Science 2000, 288:1769-1772.
90. Rainville P., et al. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 1997, 277:968-971.
91. Hofbauer R.K., et al. Cortical representation of the sensory dimension of pain. J. Neurophysiol. 2001, 86:402-411.
92. Kenntner-Mabiala R., et al. Distinct effects of attention and affect on pain perception and somatosensory evoked potentials. Biol. Psychol. 2008, 78:114-122.
93. Chapman C.R., et al. Sensory and affective dimensions of phasic pain are indistinguishable in the self-report and psychophysiology of normal laboratory subjects. J. Pain 2001, 2:279-294.
94. Fernandez E., Turk D.C. Demand characteristics underlying differential ratings of sensory versus affective components of pain. J. Behav. Med. 1994, 17:375-390.
95. Botvinick M., Cohen J. Rubber hands 'feel' touch that eyes see. Nature 1998, 391:756.