The 'where' and the 'when' of the BOLD response to pain in the insular cortex. Discussion on amplitudes and latencies

NeuroImage

Volumn 64, Issue 1, 2013, Pages 466-475

  Pomares, Florence B ^a,b,c,d   Faillenot, Isabelle ^a,b,c,d   Barral, Fabrice Guy ^b,c,d   Peyron, Roland ^a,b,c,d  

^a LYON NEUROSCIENCE RESEARCH CENTER   (France)

^b UNIVERSITÉ DE LYON   (France)

^c UNIVERSITÉ JEAN MONNET   (France)

^d UNIVERSITY HOSPITAL OF SAINT ETIENNE   (France)

Author keywords

FMRI; HRF; Insular cortex; Laser stimulation; Pain

Indexed keywords

ADULT; AMPLITUDE MODULATION; ARTICLE; BOLD SIGNAL; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; INSULA; LATENT PERIOD; MALE; NERVE CONDUCTION; NORMAL HUMAN; PAIN; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; SAMPLING;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; HUMANS; MALE; NERVE NET; PAIN PERCEPTION; REACTION TIME;

EID: 84867477220     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.09.038     Document Type: Article

References (67)

1. Afif A., Mertens P. Description of sulcal organization of the insular cortex. Surg. Radiol. Anat. 2010, 32:491-498.
2. Aguirre G., Zarahn E., D'esposito M. The variability of human, BOLD hemodynamic responses. Neuroimage 1998, 8:360-369.
3. Apkarian A., Bushnell M., Treede R.-D., Zubieta J.-K. Human brain mechanisms of pain perception and regulation in health and disease. Eur. J. Pain 2005, 9:463-484.
4. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851. 10.1016/j.neuroimage.2005.02.018.
5. Baliki M., Geha P., Apkarian A. Parsing pain perception between nociceptive representation and magnitude estimation. J. Neurophysiol. 2009, 101:875-887.
6. Baumgärtner U., Iannetti G., Zambreanu L., Stoeter P., Treede R.-D., Tracey I. Multiple somatotopic representations of heat and mechanical pain in the operculo-insular cortex: a high-resolution fMRI study. J. Neurophysiol. 2010, 104:2863-2872.
7. Boly M., Balteau E., Schnakers C., Degueldre C., Moonen G., Luxen A., Phillips C., et al. Baseline brain activity fluctuations predict somatosensory perception in humans. PNAS 2007, 104:12187-12192.
8. Bornhövd K., Quante M., Glauche V., Bromm B., Weiller C., Büchel C. Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. Brain 2002, 125:1326-1336.
9. Brinkmeyer J., Mobascher A., Warbrick T., Musso F., Wittsack H.-J., Saleh A., Schnitzler A., et al. Dynamic EEG-informed fMRI modeling of the pain matrix using 20-ms root mean square segments. Hum. Brain Mapp. 2010, 31:1702-1712.
10. Brooks J., Tracey I. From nociception to pain perception: imaging the spinal and supraspinal pathways. J. Anat. 2005, 207:19-33.
11. Brooks J., Tracey I. The insula: a multidimensional integration site for pain. Pain 2007, 128:1-2.
12. Büchel C., Bornhovd K., Quante M., Glauche V., Bromm B., Weiller C. 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. 2002, 22:970-976.
13. Calhoun V., Stevens M., Pearlson G., Kiehl K. fMRI analysis with the general linear model: removal of latency-induced amplitude bias by incorporation of hemodynamic derivative terms. Neuroimage 2004, 22:252-257.
14. Casey K.L., Morrow T.J., Lorenz J., Minoshima S. Temporal and spatial dynamics of human forebrain activity during heat pain: analysis by positron emission tomography. J. Neurophysiol. 2001, 85:951-959.
15. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011, 55:8-23.
16. Chambers and colleagues Bell Laboratories. http://www.r-project.org.
17. Chen J.I., Ha B., Bushnell M.C., Pike B., Duncan G.H. Differentiating noxious and innocuous-related activation of human somatosensory cortices using temporal analysis of fMRI. J. Neurophysiol. 2002, 88:464-474.
18. Chen L., Dillenburger B., Wang F., Friedman R., Avison M. High-resolution functional magnetic resonance imaging mapping of noxious heat and tactile activations along the central sulcus in New World monkeys. Pain 2011, 152:522-532.
19. Coghill R., Sang C., Maisog J., Iadarola M. Pain intensity processing within the human brain: a bilateral, distributed mechanism. J. Neurophysiol. 1999, 82:1934-1943.
20. Coghill R., McHaffie J.G., Yen Y.F. Neural correlates of interindividual differences in the subjective experience of pain. PNAS 2003, 8:8538-8542.
21. Craig A., Zhang E.-T. Retrograde analyses of spinothalamic projections in the macaque monkey: input to posterolateral thalamus. J. Comp. Neurol. 2006, 499:953-964.
22. Craig A.D., Chen K., Bandy D., Reiman E.M. Thermosensory activation of insular cortex. Nat. Neurosci. 2000, 3:184-190.
23. Dale A. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 1999, 8:109-114.
24. Eickhoff S., Amunts K., Mohlberg H., Zilles K. The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. Cereb. Cortex 2006, 16:268-279.
25. Eickhoff S., Schleicher A., Zilles K., Amunts K. The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cereb Cortex. 2006, 16:254-267.
26. Friston K., Stephan K., Lund T., Morcom A., Kiebel S. Mixed-effects and fMRI studies. Neuroimage 2005, 24:244-252.
27. Frot M., Mauguière F. Dual representation of pain in the operculo-insular cortex in humans. Brain 2003, 126:438-450.
28. Frot M., Magnin M., Maugière F., Garcia-Larrea L. Human SII and posterior insula differently encode thermal laser stimuli. Cereb. Cortex 2007, 17:610-620.
29. Garcia-Larrea L., Perchet C., Creac'h C., Convers P., Peyron R., Laurent B., Mauguière F., Magnin M. Operculo-insular pain (parasylvian pain): a distinct central pain syndrome. Brain 2010, 133:2528-2539.
30. Handwerker D., Ollinger J., D'Esposito M. Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses. Neuroimage 2004, 21:1639-1651.
31. Henson R. Analysis of fMRI time series: linear time-invariant models, event-related fMRI, and optimal experimental design. Human Brain Function 2003, 793-823. Elsevier, San Diego (CA). 2nd ed. R. Frackowiack (Ed.).
32. Henson R., Price C., Rugg M., Turner R., Friston K. Detecting latency differences in event-related BOLD responses: application to words versus nonwords and initial versus repeated face presentations. Neuroimage 2002, 15:83-97.
33. Iannetti G.D., Mouraux A. From the neuromatrix to the pain matrix (and back). Exp. Brain Res. 2010, 205:1-12.
34. Isnard J., Magnin M., Jung J., Mauguière F., Garcia-Larrea L. Does the insula tell our brain that we are in pain?. Pain 2011, 152:946-951.
35. Kurth F., Eickhoff S., Schleicher A., Hoemke L., Zilles K., Amunts K. Cytoarchitecture and probabilistic maps of the human posterior insular cortex. Cereb. Cortex 2010, 20:1448-1461.
36. Kurth F., Zilles K., Fox P., Laird A., Eickhoff S. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 2010, 214:519-534.
37. Legrain V., Iannetti G., Plaghki L., Mouraux A. The pain matrix reloaded: a salience detection system for the body. Prog. Neurobiol. 2010, 93:111-124.
38. Liang M., Mouraux A., Iannetti G.D. Parallel processing of nociceptive and non-nociceptive somatosensory information in the human primary and secondary somatosensory cortices: evidence from dynamic causal modeling of functional magnetic resonance imaging data. J. Neurosci. 2011, 31:8976-8985.
39. Lindquist M., Wager T. Validity and power in hemodynamic response modeling: a comparison study and a new approach. Hum. Brain Mapp. 2007, 28:764-784.
40. López-Solà M., Pujol J., Hernández-Ribas R., Harrison B., Ortiz H., Soriano-Mas C., Deus J., Menchon J.M., Vallejo J., Cardoner N. Dynamic assessment of the right lateral frontal cortex response to painful stimulation. Neuroimage 2010, 50:1177-1187.
41. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
42. Mazzola L., Isnard J., Peyron R., Guénot M., Mauguière F. Somatotopic organization of pain responses to direct electrical stimulation of the human insular cortex. Pain 2009, 146:99-104.
43. Mazzola L., Isnard J., Peyron R., Mauguière F. Stimulation of the human cortex and the experience of pain: Wilder Penfield's observations revisited. Brain 2011, 1-10. 10.1093/brain/awr265.
44. Mazzola L., Faillenot I., Barral F.G., Mauguière F., Peyron R. Spatial segregation of somato-sensory and pain activations in the human operculo-insular cortex. Neuroimage 2012, 60:409-418.
45. Mobascher A., Brinkmeyer J., Warbrick T., Musso F., Wittsack H.J., Saleh A., Schnitzler A., et al. Laser-evoked potential P2 single-trial amplitudes covary with the fMRI BOLD response in the medial pain system and interconnected subcortical structures. Neuroimage 2009, 45:917-926.
46. Mobascher A., Brinkmeyer J., Warbrick T., Musso F., Schlemper V., Wittsack H.J., Saleh A., et al. Brain activation patterns underlying fast habituation to painful laser stimuli. Int. J. Psychophysiol. 2010, 75:16-24.
47. Moulton E., Keaser M., Gullapalli R., Greenspan J. Regional intensive and temporal patterns of functional MRI activation distinguishing noxious and innocuous contact heat. J. Neurophysiol. 2005, 93:2183-2193.
48. Moulton E., Pendse G., Becerra L., Borsook D. BOLD responses in somatosensory cortices better reflect heat sensation than pain. J. Neurosci. 2012, 32(17):6024-6031.
49. Mouraux A., Iannetti G. Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. J. Neurophysiol. 2009, 101:3258-3269.
50. Mouraux A., Diukova A., Lee M., Wise R., Iannetti G. A multisensory investigation of the functional significance of the 'pain matrix'. Neuroimage 2011, 54:2237-2249.
51. Oertel B.G., Preibisch C., Martin T., Walter C., Gamer M., Deichmann R., Lötsch J. Separating brain processing of pain from that of stimulus intensity. Hum. Brain Mapp. 2011, 10.1002/hbm.21256.
52. Oldfield R. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
53. Optseq Software http://surfer.nmr.mgh.harvard.edu/optseq.
54. Peltz E., Seifert F., DeCol R., Dörfler A., Schwab S., Maihöfner C. Functional connectivity of the human insular cortex during noxious and innocuous thermal stimulation. Neuroimage 2011, 54:1324-1335.
55. Peyron R., Laurent B., García-Larrea L. Functional imaging of brain responses to pain. A review and meta-analysis. Clin. Neurophysiol. 2000, 30:263-288.
56. Plaghki L., Mouraux A. How do we selectively activate skin nociceptors with a high power infrared laser? Physiology and biophysics of laser stimulation. Clin. Neurophysiol. 2003, 33:269-277.
57. Ploner M., Lee M.C., Wiech K., Bingel U., Tracey I. Prestimulus functional connectivity determines pain perception in humans. PNAS. 2010, 107:355-360.
58. Psychology Software Tools http://www.pstnet.com.
59. Schoedel A., Zimmermann K., Handwerker H., Forster C. The influence of simultaneous ratings on cortical BOLD effects during painful and non-painful stimulation. Pain 2008, 135:131-141.
60. Steffener J., Tabert M., Reuben A., Stern Y. Investigating hemodynamic response variability at the group level using basis functions. Neuroimage 2010, 49:2113-2122. www.sites.google.com/steffener.
61. Tracey I., Mantyh P.W. The cerebral signature for pain perception and its modulation. Neuron 2007, 55:377-391.
62. Türe U., Yasargil M.G., Al-Mefty O., Yasargil D.C. Arteries of the insula. J. Neurosurg. 2000, 92:676-687.
63. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
64. Upadhyay J., Pendse G., Anderson J., Schwarz A., Baumgartner R., Coimbra A., Bishop J., Knudsen J., George E., Grachev I., Iyengar S., Bleakman D., Hargreaves R., Borsook D., Becerra L. Improved characterization of BOLD responses for evoked sensory stimuli. Neuroimage 2010, 49:2275-2286.
65. Vogt B.A. Pain and emotion interactions in subregions of the cingulate gyrus. Nat. Rev. Neurosci. 2005, 6:533-544.
66. Vogt B.A., Berger G.R., Derbyshire S.W. Structural and functional dichotomy of human midcingulate cortex. Eur. J. Neurosci. 2003, 18:3134-3144.
67. Wiech K., Lin C.-S., Brodersen K.H., Bingel U., Ploner M., Tracey I. Anterior insula integrates information about salience into perceptual decisions about pain. J. Neurosci. 2010, 30:16324-16331.