High density of nicotinic receptors in the cingulo-insular network

NeuroImage

Volumn 79, Issue , 2013, Pages 42-51

  Picard, Fabienne ^a   Sadaghiani, Sepideh ^b   Leroy, Claire ^c   Courvoisier, Delphine S ^a   Maroy, Renaud ^c   Bottlaender, Michel ^c,d  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^d DIF   (France)

Author keywords

Cingulate cortex; F A 85380; Insula; Nicotinic receptor; PET; Salience

Indexed keywords

NICOTINIC RECEPTOR ALPHA4BETA2;

ADULT; ANTERIOR CINGULATE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DEFAULT MODE NETWORK; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IN VIVO STUDY; INSULA; LEFT HEMISPHERE; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RECEPTOR DENSITY; RIGHT HEMISPHERE; SIGNAL TRANSDUCTION; THALAMUS;

ADULT; CEREBRAL CORTEX; GYRUS CINGULI; HUMANS; MALE; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, NICOTINIC; TISSUE DISTRIBUTION;

EID: 84877894037     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.04.074     Document Type: Article

References (85)

1. Aleksandrov V.G., Aleksandrova N.P., Bagaev V.A. Identification of a respiratory related area in the rat insular cortex. Can. J. Physiol. Pharmacol. 2000, 78:582-586.
2. Alkondon M., Pereira E.F., Eisenberg H.M., Albuquerque E.X. Nicotinic receptor activation in human cerebral cortical interneurons: a mechanism for inhibition and disinhibition of neuronal networks. J. Neurosci. 2000, 20:66-75.
3. An X., Bandler R., Ongur D., Price J.L. Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys. J. Comp. Neurol. 1998, 401:455-479.
4. Anderson S.M., Brunzell D.H. Low dose nicotine and antagonism of beta2 subunit containing nicotinic acetylcholine receptors have similar effects on affective behavior in mice. PLoS One 2012, 7:e48665.
5. Blum A.S. Respiratory physiology of seizures. J. Clin. Neurophysiol. 2009, 26:309-315.
6. Brody A.L. Functional brain imaging of tobacco use and dependence. J. Psychiatr. Res. 2006, 40:404-418.
7. Brown D.C., Nichols J.A., Thomas F., Dinh L., Atzori M. Nicotinic modulation of auditory attentional shift in the rat. Behav. Brain Res. 2010, 210:273-279.
8. Chang L.J., Yarkoni T., Khaw M.W., Sanfey A.G. Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb. Cortex 2013, 23:739-749.
9. Changeux J.P. Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat. Rev. Neurosci. 2010, 11:389-401.
10. Chefer S.I., Horti A.G., Koren A.O., Gundisch D., Links J.M., Kurian V., Dannals R.F., Mukhin A.G., London E.D. 2-[18F]F-A-85380: a PET radioligand for alpha4beta2 nicotinic acetylcholine receptors. Neuroreport 1999, 10:2715-2721.
11. Contreras M., Ceric F., Torrealba F. Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 2007, 318:655-658.
12. Craig A.D. How do you feel-now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
13. Critchley H.D., Wiens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 2004, 7:189-195.
14. Dani J.A. Overview of nicotinic receptors and their roles in the central nervous system. Biol. Psychiatry 2001, 49:166-174.
15. Dani J.A., Bertrand D. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 2007, 47:699-729.
16. Dobesberger J., Ortler M., Unterberger I., Walser G., Falkenstetter T., Bodner T., Benke T., Bale R., Fiegele T., Donnemiller E., Gotwald T., Trinka E. Successful surgical treatment of insular epilepsy with nocturnal hypermotor seizures. Epilepsia 2008, 49:159-162.
17. Doll F., Dolci L., Valette H., Hinnen F., Vaufrey F., Guenther I., Fuseau C., Coulon C., Bottlaender M., Crouzel C. Synthesis and nicotinic acetylcholine receptor in vivo binding properties of 2-fluoro-3-[2(S)-2-azetidinylmethoxy]pyridine: a new positron emission tomography ligand for nicotinic receptors. J. Med. Chem. 1999, 42:2251-2259.
18. Domino E.F., Riskalla M., Zhang Y., Kim E. Effects of tobacco smoking on the topographic EEG II. Prog. Neuropsychopharmacol. Biol. Psychiatry 1992, 16:463-482.
19. Dosenbach N.U., Visscher K.M., Palmer E.D., Miezin F.M., Wenger K.K., Kang H.C., Burgund E.D., Grimes A.L., Schlaggar B.L., Petersen S.E. A core system for the implementation of task sets. Neuron 2006, 50:799-812.
20. Dosenbach N.U., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A., Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E., Schlaggar B.L., Petersen S.E. Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11073-11078.
21. Drake M.J., Fowler C.J., Griffiths D., Mayer E., Paton J.F., Birder L. Neural control of the lower urinary and gastrointestinal tracts: supraspinal CNS mechanisms. Neurourol. Urodyn. 2010, 29:119-127.
22. Evans K.C., Banzett R.B., Adams L., McKay L., Frackowiak R.S., Corfield D.R. BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger. J. Neurophysiol. 2002, 88:1500-1511.
23. Fadel J.R. Regulation of cortical acetylcholine release: insights from in vivo microdialysis studies. Behav. Brain Res. 2011, 221:527-536.
24. Frouin V., Comtat C., Reilhac A., Gregoire M.C. Correction of partial-volume effect for PET striatal imaging: fast implementation and study of robustness. J. Nucl. Med. 2002, 43:1715-1726.
25. Gallezot J.D., Bottlaender M., Gregoire M.C., Roumenov D., Deverre J.R., Coulon C., Ottaviani M., Dolle F., Syrota A., Valette H. In vivo imaging of human cerebral nicotinic acetylcholine receptors with 2-18F-fluoro-A-85380 and PET. J. Nucl. Med. 2005, 46:240-247.
26. Gallezot J.D., Bottlaender M.A., Delforge J., Valette H., Saba W., Dolle F., Coulon C.M., Ottaviani M.P., Hinnen F., Syrota A., Gregoire M.C. Quantification of cerebral nicotinic acetylcholine receptors by PET using 2-[18F]fluoro-A-85380 and the multiinjection approach. J. Cereb. Blood Flow Metab. 2008, 28:172-189.
27. Gao Y., Kuwabara H., Spivak C.E., Xiao Y., Kellar K., Ravert H.T., Kumar A., Alexander M., Hilton J., Wong D.F., Dannals R.F., Horti A.G. Discovery of (-)-7-methyl-2-exo-[3'-(6-[18F]fluoropyridin-2-yl)-5'-pyridinyl]-7-azabicy clo[2.2.1]heptane, a radiolabeled antagonist for cerebral nicotinic acetylcholine receptor (alpha4beta2-nAChR) with optimal positron emission tomography imaging properties. J. Med. Chem. 2008, 51:4751-4764.
28. Goldstein R.Z., Craig A.D., Bechara A., Garavan H., Childress A.R., Paulus M.P., Volkow N.D. The neurocircuitry of impaired insight in drug addiction. Trends Cogn. Sci. 2009, 13:372-380.
29. Gray M.A., Critchley H.D. Interoceptive basis to craving. Neuron 2007, 54:183-186.
30. Guenot M., Isnard J. Epilepsy and insula. Neurochirurgie 2008, 54:374-381.
31. Hasenkamp W., Wilson-Mendenhall C.D., Duncan E., Barsalou L.W. Mind wandering and attention during focused meditation: a fine-grained temporal analysis of fluctuating cognitive states. Neuroimage 2012, 59:750-760.
32. Horti A.G., Scheffel U., Koren A.O., Ravert H.T., Mathews W.B., Musachio J.L., Finley P.A., London E.D., Dannals R.F. 2-[18F]Fluoro-A-85380, an in vivo tracer for the nicotinic acetylcholine receptors. Nucl. Med. Biol. 1998, 25:599-603.
33. Impey D., Chique-Alfonzo M., Shah D., Fisher D.J., Knott V.J. Effects of nicotine on visuospatial attentional orienting in non-smokers. Pharmacol. Biochem. Behav. 2013, 106:1-7.
34. Isnard J., Guenot M., Sindou M., Mauguiere F. Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 2004, 45:1079-1090.
35. Jones S.E. Imaging for autonomic dysfunction. Cleve. Clin. J. Med. 2011, 78(Suppl. 1):S69-S74.
36. Kaido T., Otsuki T., Nakama H., Kaneko Y., Kubota Y., Sugai K., Saito O. Complex behavioral automatism arising from insular cortex. Epilepsy Behav. 2006, 8:315-319.
37. Kimes A.S., Horti A.G., London E.D., Chefer S.I., Contoreggi C., Ernst M., Friello P., Koren A.O., Kurian V., Matochik J.A., Pavlova O., Vaupel D.B., Mukhin A.G. 2-[18F]F-A-85380: PET imaging of brain nicotinic acetylcholine receptors and whole body distribution in humans. FASEB J. 2003, 17:1331-1333.
38. Knott V.J. Dynamic EEG changes during cigarette smoking. Neuropsychobiology 1988, 19:54-60.
39. Knott V.J., Harr A., Ilivitsky V., Mahoney C. The cholinergic basis of the smoking-induced EEG activation profile. Neuropsychobiology 1998, 38:97-107.
40. Knott V., Bosman M., Mahoney C., Ilivitsky V., Quirt K. Transdermal nicotine: single dose effects on mood, EEG, performance, and event-related potentials. Pharmacol. Biochem. Behav. 1999, 63:253-261.
41. Kobiella A., Ulshofer D.E., Vollmert C., Vollstadt-Klein S., Buhler M., Esslinger C., Smolka M.N. Nicotine increases neural response to unpleasant stimuli and anxiety in non-smokers. Addict. Biol. 2011, 16:285-295.
42. Kurth F., Zilles K., Fox P.T., Laird A.R., Eickhoff S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 2010, 214:519-534.
43. Lamm C., Singer T. The role of anterior insular cortex in social emotions. Brain Struct. Funct. 2010, 214:579-591.
44. Li M.D., Burmeister M. New insights into the genetics of addiction. Nat. Rev. Genet. 2009, 10:225-231.
45. Lindgren M., Molander L., Verbaan C., Lunell E., Rosen I. Electroencephalographic effects of intravenous nicotine-a dose-response study. Psychopharmacology (Berl) 1999, 145:342-350.
46. Mancuso G., Warburton D.M., Melen M., Sherwood N., Tirelli E. Selective effects of nicotine on attentional processes. Psychopharmacology (Berl) 1999, 146:199-204.
47. Meinke A., Thiel C.M., Fink G.R. Effects of nicotine on visuo-spatial selective attention as indexed by event-related potentials. Neuroscience 2006, 141:201-212.
48. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
49. Mesulam M.M. Structure and function of cholinergic pathways in the cerebral cortex, limbic system, basal ganglia, and thalamus of the human brain. Psychopharmacology: The Fourth Generation of Progress 1995, 135-146. Raven Press, New York. F.E. Bloom, D.J. Kupfer (Eds.).
50. Mitkovski S., Villemagne V.L., Novakovic K.E., O'Keefe G., Tochon-Danguy H., Mulligan R.S., Dickinson K.L., Saunder T., Gregoire M.C., Bottlaender M., Dolle F., Rowe C.C. Simplified quantification of nicotinic receptors with 2[18F]F-A-85380 PET. Nucl. Med. Biol. 2005, 32:585-591.
51. Mobbs D., Marchant J.L., Hassabis D., Seymour B., Tan G., Gray M., Petrovic P., Dolan R.J., Frith C.D. From threat to fear: the neural organization of defensive fear systems in humans. J. Neurosci. 2009, 29:12236-12243.
52. Moser N., Mechawar N., Jones I., Gochberg-Sarver A., Orr-Urtreger A., Plomann M., Salas R., Molles B., Marubio L., Roth U., Maskos U., Winzer-Serhan U., Bourgeois J.P., Le Sourd A.M., De Biasi M., Schroder H., Lindstrom J., Maelicke A., Changeux J.P., Wevers A. Evaluating the suitability of nicotinic acetylcholine receptor antibodies for standard immunodetection procedures. J. Neurochem. 2007, 102:479-492.
53. Mosteller F., Tukey J. Two- and more-way tables. Data Analysis and Regression, a Second Course in Statistics 1977, 165-202. Addison-Wesley Publishing Company, Reading, MA.
54. Mutschler I., Wieckhorst B., Kowalevski S., Derix J., Wentlandt J., Schulze-Bonhage A., Ball T. Functional organization of the human anterior insular cortex. Neurosci. Lett. 2009, 457:66-70.
55. Naqvi N.H., Rudrauf D., Damasio H., Bechara A. Damage to the insula disrupts addiction to cigarette smoking. Science 2007, 315:531-534.
56. Nelson S.M., Dosenbach N.U., Cohen A.L., Wheeler M.E., Schlaggar B.L., Petersen S.E. Role of the anterior insula in task-level control and focal attention. Brain Struct. Funct. 2010, 214:669-680.
57. Newhouse P., Kellar K., Aisen P., White H., Wesnes K., Coderre E., Pfaff A., Wilkins H., Howard D., Levin E.D. Nicotine treatment of mild cognitive impairment: a 6-month double-blind pilot clinical trial. Neurology 2012, 78:91-101.
58. Oppenheimer S. Cortical control of the heart. Cleve. Clin. J. Med. 2007, 74(Suppl. 1):S27-S29.
59. Penfield W., Faulk M.E. The insula; further observations on its function. Brain 1955, 78:445-470.
60. Perry D.C., Xiao Y., Nguyen H.N., Musachio J.L., Davila-Garcia M.I., Kellar K.J. Measuring nicotinic receptors with characteristics of alpha4beta2, alpha3beta2 and alpha3beta4 subtypes in rat tissues by autoradiography. J. Neurochem. 2002, 82:468-481.
61. Petrovsky N., Ettinger U., Quednow B.B., Walter H., Schnell K., Kessler H., Mossner R., Maier W., Wagner M. Nicotine differentially modulates antisaccade performance in healthy male non-smoking volunteers stratified for low and high accuracy. Psychopharmacology (Berl) 2012, 221:27-38.
62. Picard F., Brodtkorb E. Familial frontal lobe epilepsies. Epilepsy: a Comprehensive Textbook 2007, 2495-2502. Lippincott Williams & Wilkins, Philadelphia. J. Engel, T.A. Pedley (Eds.).
63. Picard F., Baulac S., Kahane P., Hirsch E., Sebastianelli R., Thomas P., Vigevano F., Genton P., Guerrini R., Gericke C.A., An I., Rudolf G., Herman A., Brice A., Marescaux C., LeGuern E. Dominant partial epilepsies. A clinical, electrophysiological and genetic study of 19 European families. Brain 2000, 123(Pt 6):1247-1262.
64. Picard F., Bruel D., Servent D., Saba W., Fruchart-Gaillard C., Schollhorn-Peyronneau M.A., Roumenov D., Brodtkorb E., Zuberi S., Gambardella A., Steinborn B., Hufnagel A., Valette H., Bottlaender M. Alteration of the in vivo nicotinic receptor density in ADNFLE patients: a PET study. Brain 2006, 129:2047-2060.
65. Poltavski D.V., Petros T. Effects of transdermal nicotine on attention in adult non-smokers with and without attentional deficits. Physiol. Behav. 2006, 87:614-624.
66. Power J.D., Petersen S.E. Control-related systems in the human brain. Curr. Opin. Neurobiol. 2013, 23:223-228.
67. Power J.D., Cohen A.L., Nelson S.M., Wig G.S., Barnes K.A., Church J.A., Vogel A.C., Laumann T.O., Miezin F.M., Schlaggar B.L., Petersen S.E. Functional network organization of the human brain. Neuron 2011, 72:665-678.
68. Rose E.J., Ross T.J., Kurup P.K., Stein E.A. Nicotine modulation of information processing is not limited to input (attention) but extends to output (intention). Psychopharmacology (Berl) 2010, 209:291-302.
69. Rousset O.G., Ma Y., Evans A.C. Correction for partial volume effects in PET: principle and validation. J. Nucl. Med. 1998, 39:904-911.
70. Rubboli F., Court J.A., Sala C., Morris C., Perry E., Clementi F. Distribution of neuronal nicotinic receptor subunits in human brain. Neurochem. Int. 1994, 25:69-71.
71. Ryvlin P., Minotti L., Demarquay G., Hirsch E., Arzimanoglou A., Hoffman D., Guenot M., Picard F., Rheims S., Kahane P. Nocturnal hypermotor seizures, suggesting frontal lobe epilepsy, can originate in the insula. Epilepsia 2006, 47:755-765.
72. Sadaghiani S., Hesselmann G., Friston K.J., Kleinschmidt A. The relation of ongoing brain activity, evoked neural responses, and cognition. Front. Syst. Neurosci. 2010, 4:20.
73. Sadaghiani S., Scheeringa R., Lehongre K., Morillon B., Giraud A.L., Kleinschmidt A. Intrinsic connectivity networks, alpha oscillations, and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J. Neurosci. 2010, 30:10243-10250.
74. Sadaghiani S., Scheeringa R., Lehongre K., Morillon B., Giraud A.L., D'Esposito M., Kleinschmidt A. Alpha-band phase synchrony is related to activity in the fronto-parietal adaptive control network. J. Neurosci. 2012, 32:14305-14310.
75. Schroder H., Zilles K., Maelicke A., Hajos F. Immunohisto- and cytochemical localization of cortical nicotinic cholinoceptors in rat and man. Brain Res. 1989, 502:287-295.
76. Seeley W.W. Anterior insula degeneration in frontotemporal dementia. Brain Struct. Funct. 2010, 214:465-475.
77. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
78. Smith S.M., Fox P.T., Miller K.L., Glahn D.C., Fox P.M., Mackay C.E., Filippini N., Watkins K.E., Toro R., Laird A.R., Beckmann C.F. Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13040-13045.
79. Soros P., Hachinski V. Cardiovascular and neurological causes of sudden death after ischaemic stroke. Lancet Neurol. 2012, 11:179-188.
80. Sturm W., Longoni F., Fimm B., Dietrich T., Weis S., Kemna S., Herzog H., Willmes K. Network for auditory intrinsic alertness: a PET study. Neuropsychologia 2004, 42:563-568.
81. Valette H., Bottlaender M., Dolle F., Guenther I., Fuseau C., Coulon C., Ottaviani M., Crouzel C. Imaging central nicotinic acetylcholine receptors in baboons with [18F]fluoro-A-85380. J. Nucl. Med. 1999, 40:1374-1380.
82. Wevers A. Localisation of pre- and postsynaptic cholinergic markers in the human brain. Behav. Brain Res. 2011, 221:341-355.
83. Yasui Y., Breder C.D., Saper C.B., Cechetto D.F. Autonomic responses and efferent pathways from the insular cortex in the rat. J. Comp. Neurol. 1991, 303:355-374.
84. Zhang H., Yao Q., Zhao X., Jin X., Wang C., Guo H., You Y., Wang H., Gao G. A hypermotor seizure with a focal orbital frontal lesion originating in the insula: a case report. Epilepsy Res. 2008, 82:211-214.
85. Zilles K., Palomero-Gallagher N., Schleicher A. Transmitter receptors and functional anatomy of the cerebral cortex. J. Anat. 2004, 205:417-432.