Processing of nociceptive input from posterior to anterior insula in humans

Human Brain Mapping

Volumn 35, Issue 11, 2014, Pages 5486-5499

  Frot, Maud ^a,b   Faillenot, Isabelle ^a,c   Mauguière, François ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ LYON 1   (France)

^c UNIVERSITY HOSPITAL OF SAINT ETIENNE   (France)

^d HOSPICES CIVILS DE LYON   (France)

Author keywords

Humans; Insula; Intracerebral recordings; Laser evoked potentials; Pain

Indexed keywords

ADOLESCENT; ADULT; ANTERIOR INSULA; ARTICLE; CLINICAL ARTICLE; CORTICAL ELECTRODE; EPILEPSY; EVOKED RESPONSE; FEMALE; FUNCTIONAL NEUROIMAGING; HEAT; HUMAN; MALE; NEUROANATOMY; NOCICEPTION; NOCICEPTIVE STIMULATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PAIN; PAIN THRESHOLD; POSTERIOR INSULA; PRIORITY JOURNAL; ADVERSE EFFECTS; BRAIN ANGIOGRAPHY; BRAIN CORTEX; BRAIN MAPPING; ELECTRODE IMPLANT; HEMISPHERIC DOMINANCE; LASER; MIDDLE AGED; NERVE CELL NETWORK; PHYSIOLOGY; RADIOGRAPHY; YOUNG ADULT;

ADOLESCENT; ADULT; BRAIN MAPPING; CEREBRAL ANGIOGRAPHY; CEREBRAL CORTEX; ELECTRODES, IMPLANTED; EVOKED POTENTIALS; FEMALE; FUNCTIONAL LATERALITY; HUMANS; LASERS; MALE; MIDDLE AGED; NERVE NET; NOCICEPTION; YOUNG ADULT;

EID: 84911986657     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22565     Document Type: Article

References (58)

1. Almashaikhi T, Rheims S, Ostrowsky-Coste K, Montavont A, Jung J, De Bellescize J, Arzimanoglou A, Keo Kosal P, Guénot M, Bertrand O, Ryvlin P (2013): Intrainsular functional connectivity in human. Hum Brain Mapp. doi: 10.1002/hbm.22366.
2. 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.
3. Ashburner J, Friston KJ (2005): Unified segmentation. Neuroimage 26:839-851.
4. Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229-244.
5. Berthier M, Starkstein S, Leiguarda R (1988) Asymbolia for pain: A sensory-limbic disconnection syndrome. Ann Neurol 24:41-49.
6. Brett M, Anton JL, Valabregue R, Poline JB (2002): Region of interest analysis using an SPM toolbox [abstract] Presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2-6, 2002, Sendai, Japan.
7. Brooks JC, Zambreanu L, Godinez A, Craig AD, Tracey I (2005): Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging. Neuroimage 27: 201-209.
8. Cauda F, D'Agata F, Sacco K, Duca S, Geminiani G, Vercelli A (2011): Functional connectivity of the insula in the resting brain. Neuroimage 55:8-23.
9. Cerliani L, Thomas RM, Jbabdi S, Siero JC, Nanetti L, Crippa A, Gazzola V, D'Arceuil H, Keysers C (2012): Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex. Hum Brain Mapp 33:2005-2034.
10. Cloutman LL, Binney RJ, Drakesmith M, Parker GJ, Lambon Ralph MA (2012) The variation of function across the human insula mirrors its patterns of structural connectivity: Evidence from in vivo probabilistic tractography. Neuroimage 59:3514-3521.
11. Corradi-Dell'Acqua C, Hofstetter C, Vuilleumier P (2011): Felt and seen pain evoke the same local patterns of cortical activity in insular and cingulate cortex. J Neurosci 31:17996-18006.
12. Craig AD (2002): How do you feel? Interoception: The sense of the physiological condition of the body. Nat Rev Neurosci 3:655-666.
13. Craig AD, Bushnell MC, Zhang ET, Blomqvist A (1994): A thalamic nucleus specific for pain and temperature sensation. Nature 372:770-773.
14. Cruccu G, Aminoff MJ, Curio G, Guerit JM, Kakigi R, Mauguière F, Rossini PM, Treede RD, Garcia-Larrea L (2008) Recommendations for the clinical use of somatosensory-evoked potentials. Clin Neurophysiol 119:1705-1719.
15. Duerden EG, Albanese MC (2011) Localization of pain-related brain activation: A meta-analysis of neuroimaging data. Hum Brain Mapp 34:109-149.
16. 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.
17. Eickoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325-1335.
18. Eickhoff SB, Heim S, Zilles K, Amunts K (2006): Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. NeuroImage 32:570-582.
19. Eickhoff SB, Jbabdi S, Caspers S, Laird AR, Fox PT, Zilles K, Behrens TEJ (2010): Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J Neurosci 30:6409-6421.
20. Friedman DP, Murray EA, O'Neill JB, Mishkin M (1986): Cortical connections of the somatosensory fields of the lateral sulcus of macaques: Evidence for a corticolimbic pathway for touch. J Comp Neurol 252:323-347.
21. Frot M, Mauguière F (2003): Dual representation of pain in the operculo-insular cortex in humans. Brain 126:438-450.
22. Frot M, Magnin M, Mauguière F, Garcia-Larrea L (2007): Human SII and insula differently encode thermal stimuli. Cereb Cortex 17:610-620.
23. Frot M, Magnin M, Mauguière F, Garcia-Larrea L (2012): Cortical representation of pain in primary sensory-motor areas (S1/M1)-a study using intracortical recordings in humans. Hum Brain Mapp Jun 15. doi: 10.1002/hbm.22097
24. Garcia-Larrea L, Peyron R (2013): Pain matrices and neuropathic pain matrices: A review. Pain 154 (Suppl 1):S29-S43. doi: 10.1016/j.pain.2013.09.001.
25. Garcia-Larrea L, Frot M, Valeriani M (2003) Brain generators of laser-evoked potentials: From dipoles to functional significance. Neurophysiol Clin 33:279-292.
26. Garcia-Larrea L, Perchet C, Creac'h C, Convers P, Peyron R, Laurent B, Mauguière F, Magnin M (2010): Operculo-insular pain (parasylvian pain): A distinct central pain syndrome. Brain 133:2528-2539.
27. Greffrath W, Baumgärtner U, Treede RD (2007): Peripheral and central components of habituation of heat pain perception and evoked potentials in humans. Pain 132:301-311.
28. Henderson LA, Gandevia SC, Macefield VG (2007): Somatotopic organization of the processing of muscle and cutaneous pain in the left and right insula cortex: A single-trial fMRI study. Pain 128:20-30.
29. Isnard J, Guénot M, Ostrowsky K, Sindou M, Mauguière F (2000): The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 48:614-623.
30. Isnard J, Guénot M, Sindou M, Mauguière F (2004) Clinical manifestations of insular lobe seizures: A stereo electroencephalographic study. Epilepsia 45:1079-1090.
31. 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.
32. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010a): A link between the systems: Functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214(5-6):519-534.
33. Kurth F, Eickhoff SB, Schleicher A, Hoemke L, Zilles K, Amunts K (2010b): Cytoarchitecture and probabilistic maps of the human posterior insular cortex. Cereb Cortex 20:1448-1461.
34. Leandri M, Saturno M, Spadavecchia L, Iannetti GD, Cruccu G, Truini A (2006): Measurement of skin temperature after infrared laser stimulation. Neurophysiol Clin 36:207-218.
35. Mazzola L, Isnard J, Mauguière F (2006): Somatosensory and pain responses to stimulation of the second somatosensory area (SII) in humans. A comparison with SI and insular responses. Cereb Cortex 16:960-968.
36. Mazzola L, Faillenot I, Barral FG, Mauguière F, Peyron R (2012a): Spatial segregation of somato-sensory and pain activations in the human operculo-insular cortex. Neuroimage 60:409-418.
37. Mazzola L, Isnard J, Peyron R, Mauguière F (2012b): Stimulation of the human cortex and the experience of pain: Wilder Penfield's observations revisited. Brain 135:631-640.
38. Mesulam MM, Mufson EJ (1982): Insula of the old world monkey. III. Efferent cortical output and comments on function. J Comp Neurol 212:38-52.
39. Mesulam MM, Mufson EJ (1985): The insula of Reil in man and monkey. In: Peters A, Jones EG, editors. Association and Auditory Cortices. New York: Plenum. pp 179-226.
40. Moisset X, Bouhassira D (2007): Brain imaging of neuropathic pain. Neuroimage 37 (Suppl 1):S80-S88.
41. Morel A, Gallay MN, Baechler A, Wyss M, Gallay DS (2013): The human insula: Architectonic organization and postmortem MRI registration. Neuroscience 236:117-135.
42. Mufson EJ, Mesulam MM (1982): Insula of the old world monkey. II. Afferent cortical input and comments on the claustrum. J Comp Neurol 212:23-37.
43. Naidich TP, Kang E, Fatterpekar GM, Delman BN, Gultekin SH, Wolfe D, Ortiz O, Yousry I, Weismann M, Yousry TA (2004): The insula: Anatomic study and MR imaging display at 1.5 T. AJNR Am J Neuroradiol 25:222-232.
44. Nieuwenhuys R (2012): The insular cortex: A review. Prog Brain Res 195:123-163.
45. Oertel BG, Preibisch C, Martin T, Walter C, Gamer M, Deichmann R, Lötsch J (2012): Separating brain processing of pain from that of stimulus intensity. Hum Brain Mapp 33:883-894.
46. Ostrowsky K, Isnard J, Ryvlin P, Guénot M, Fischer C, Mauguière F (2000): Functional mapping of the insular cortex: Clinical implication in temporal lobe epilepsy. Epilepsia 41:681-686.
47. Ostrowsky K, Magnin M, Ryvlin P, Isnard J, Guenot M, Mauguière 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.
48. Perchet C, Godinho F, Mazza S, Frot M, Legrain V, Magnin M, Garcia-Larrea L (2008): Evoked potentials to nociceptive stimuli delivered by CO2 or Nd:YAP lasers. Clin Neurophysiol 119:2615-2622.
49. Rorden C, Brett M (2000): Stereotaxic display of brain lesions. Behav Neurol 12:191-200.
50. Schnitzler A, Ploner M (2000): Neurophysiology and functional neuroanatomy of pain perception. J Clin Neurophysiol 17:592-603.
51. Schwarz S, Greffrath W, Büsselberg D, Treede RD (2000): Inactivation and tachyphylaxis of heat-evoked inward currents in nociceptive primary sensory neurones of rats. J Physiol 528:539-549.
52. Schweinhardt P, Bushnell MC (2010): Pain imaging in health and disease-How far have we come? J Clin Invest 120:3788-3797.
53. Seltzer B, Pandya DN (1991) Post-rolandic cortical projections of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 312:625-640.
54. 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.
55. Stancak A, Fallon N (2013): Emotional modulation of experimental pain: A source imaging study of laser evoked potentials. Front Hum Neurosci 7:1-16.
56. Stancak A, Ward H, Fallon N (2013): Modulation of pain by emotional sounds: A laser-evoked potential study. Eur J Pain 17:324-335.
57. Talairach J, Tournoux P (1988): Coplanar Stereotaxic Atlas of the Human Brain. 3-Dimensional Proportional System: An approach to Cerebral Imaging. Stuttgart: Georg Thieme Verlag.
58. Wiech K, Tracey I (2009): The influence of negative emotions on pain: Behavioral effects and neural mechanisms. Neuroimage 47:987-994.