Insula Demonstrates a Non-Linear Response to Varying Demand for Cognitive Control and Weaker Resting Connectivity with the Executive Control Network in Smokers

Neuropsychopharmacology

Volumn 41, Issue 10, 2016, Pages 2557-2565

  Fedota, John R ^a   Matous, Allison L ^a   Salmeron, Betty Jo ^a   Gu, Hong ^a   Ross, Thomas J ^a   Stein, Elliot A ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN; COGNITIVE DEFECT; CONNECTOME; CONTROLLED STUDY; EXECUTIVE FUNCTION; HUMAN; INSULA; NEUROIMAGING; NONLINEAR SYSTEM; PRIORITY JOURNAL; RESTING STATE NETWORK; SALIENCE NETWORK; SMOKING; SUPERIOR FRONTAL GYRUS; ADOLESCENT; BLOOD; COGNITION DISORDERS; DIAGNOSTIC IMAGING; FEMALE; IMAGE PROCESSING; MALE; MIDDLE AGED; NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REACTION TIME; YOUNG ADULT;

OXYGEN;

ADOLESCENT; ADULT; BRAIN; COGNITION DISORDERS; EXECUTIVE FUNCTION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; REACTION TIME; SMOKING; YOUNG ADULT;

EID: 84969922419     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2016.62     Document Type: Article

References (53)

1. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005). Investigations into resting-state connectivity using independent component analysis. Philos Trans Roy Soc Lond B Biol Sci 360: 1001-1013.
2. Botvinick MM (2007). Conflict monitoring and decision making: reconciling two perspectives on anterior cingulate function. Cogn Affect Behav Neurosci 7: 356-366.
3. Brody AL, Mandelkern MA, Jarvik ME, Lee GS, Smith EC, Huang JC et al (2004). Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry 55: 77-84.
4. Buzzell GA, Fedota JR, Roberts DM, McDonald CG (2014). The N2 ERP component as an index of impaired cognitive control in smokers. Neurosci Lett 563: 61-65.
5. Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2013). Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb Cortex 23: 739-749.
6. Chen G, Saad ZS, Britton JC, Pine DS, Cox RW (2013). Linear mixed-effects modeling approach to FMRI group analysis. Neuroimage 73: 176-190.
7. Chen G, Saad ZS, Nath AR, Beauchamp MS, Cox RW (2012). FMRI group analysis combining effect estimates and their variances. Neuroimage 60: 747-765.
8. Cieslik EC, Mueller VI, Eickhoff CR, Langner R, Eickhoff SB (2015). Three key regions for supervisory attentional control: evidence from neuroimaging meta-analyses. Neurosci Biobehav Rev 48: 22-34.
9. Claus ED, Blaine SK, Filbey FM, Mayer AR, Hutchison KE (2013). Association between nicotine dependence severity, BOLD response to smoking cues, and functional connectivity. Neuropsychopharmacology 38: 2363-2372.
10. Craig ADB (2009). How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59-70.
11. de Ruiter MB, Oosterlaan J, Veltman DJ, van den Brink W, Goudriaan AE (2012). Similar hyporesponsiveness of the dorsomedial prefrontal cortex in problem gamblers and heavy smokers during an inhibitory control task. Drug Alcohol Depend 121: 81-89.
12. Droutman V, Read SJ, Bechara A (2015). Revisiting the role of the insula in addiction. Trends Cogn Sci 19: 414-420.
13. Evans DE, Park JY, Maxfield N, Drobes DJ (2009). Neurocognitive variation in smoking behavior and withdrawal: genetic and affective moderators. Genes Brain Behav 8: 86-96.
14. Fan J, Van Dam NT, Gu X, Liu X, Wang H, Tang CY et al (2014). Quantitative characterization of functional anatomical contributions to cognitive control under uncertainty. J Cogn Neurosci 26: 1490-1506.
15. Fedota JR, Stein EA (2015). Resting-state functional connectivity and nicotine addiction: prospects for biomarker development. Ann NY Acad Sci 1349: 64-82.
16. Forster SE, Carter CS, Cohen JD, Cho RY (2011). Parametric manipulation of the conflict signal and control-state adaptation. J Cogn Neurosci 23: 923-935.
17. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102: 9673-9678.
18. Franken IHA, van Strien JW, Kuijpers I (2010). Evidence for a deficit in the salience attribution to errors in smokers. Drug Alcohol Depend 106: 181-185.
19. Franklin TR, Wang Z, Wang J, Sciortino N, Harper D, Li Y et al (2007). Limbic activation to cigarette smoking cues independent of nicotine withdrawal: a perfusion fMRI study. Neuropsychopharmacology 32: 2301-2309.
20. Friedman L, Glover GH, Krenz D, Magnotta V (2006). Reducing inter-scanner variability of activation in a multicenter fMRI study: role of smoothness equalization. Neuroimage 32: 1656-1668.
21. Gallinat J, Meisenzahl E, Jacobsen LK, Kalus P, Bierbrauer J, Kienast T et al (2006). Smoking and structural brain deficits: a volumetric MR investigation. Eur J Neurosci 24: 1744-1750.
22. Goldstein RZ, Volkow ND (2011). Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12: 652-669.
23. Hahn B, Ross TJ, Yang Y, Kim I, Huestis MA, Stein EA (2007). Nicotine enhances visuospatial attention by deactivating areas of the resting brain default network. J Neurosci 27: 3477-3489.
24. Heishman SJ, Singleton EG, Crouch DJ (1996). Laboratory validation study of drug evaluation and classification program: ethanol, cocaine, and marijuana. J Anal Toxicol 20: 468-483.
25. Inzlicht M, Bartholow BD, Hirsh JB (2015). Emotional foundations of cognitive control. Trends Cogn Sci 19: 126-132.
26. Janes AC, Farmer S, Peechatka AL, Frederick B, de B, Lukas SE (2015). Insula-dorsal anterior cingulate cortex coupling is associated with enhanced brain reactivity to smoking cues. Neuropsychopharmacology 40: 1561-1568.
27. Janes AC, Pizzagalli DA, Richardt S, Frederick B, de B, Holmes AJ et al (2010). Neural substrates of attentional bias for smokingrelated cues: an FMRI study. Neuropsychopharmacology 35: 2339-2345.
28. Kalivas PW, Volkow ND (2005). The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162: 1403-1413.
29. Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, Milham MP (2008). Competition between functional brain networks mediates behavioral variability. Neuroimage 39: 527-537.
30. Klein TA, Ullsperger M, Danielmeier C (2013). Error awareness and the insula: links to neurological and psychiatric diseases. Front Hum Neurosci 7: 14.
31. Kool W, McGuire JT, Wang GJ, Botvinick MM (2013). Neural and behavioral evidence for an intrinsic cost of self-control. PLoS One 8: e72626.
32. Lerman C, Gu H, Loughead J, Ruparel K, Yang Y, Stein EA (2014). Large-scale brain network coupling predicts acute nicotine abstinence effects on craving and cognitive function. JAMA Psychiatry 71: 523-530.
33. Lubman DI, Yücel M, Pantelis C (2004). Addiction, a condition of compulsive behaviour? Neuroimaging and neuropsychological evidence of inhibitory dysregulation. Addiction 99: 1491-1502.
34. Luijten M, van Meel CS, Franken IHA (2011). Diminished error processing in smokers during smoking cue exposure. Pharmacol Biochem Behav 97: 514-520.
35. Mars RB, Sallet J, Rushworth MFS, Yeung N (eds) (2011). Neural Basis of Motivational and Cognitive Control. MIT Press: Cambridge, MA, USA. Retrieved from https://books.google.com/books?hl= en&lr=&id=A-eoYgtLmFMC&pgis =1.
36. Morales AM, Ghahremani D, Kohno M, Hellemann GS, London ED (2014). Cigarette exposure, dependence, and craving are related to insula thickness in young adult smokers. Neuropsychopharmacology 39: 1816-1822.
37. Naqvi NH, Gaznick N, Tranel D, Bechara A (2014). The insula: a critical neural substrate for craving and drug seeking under conflict and risk. Ann NY Acad Sci 1316: 53-70.
38. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007). Damage to the insula disrupts addiction to cigarette smoking. Science 315: 531-534.
39. Nee DE, Wager TD, Jonides J (2007). Interference resolution: insights from a meta-analysis of neuroimaging tasks. Cogn Affect Behav Neurosci 7: 1-17.
40. Paulus MP, Stewart JL (2014). Interoception and drug addiction. Neuropharmacology 76(Pt B): 342-350.
41. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001). A default mode of brain function. Proc Natl Acad Sci USA 98: 676-682.
42. Rass O, Fridberg DJ, O'Donnell BF (2014). Neural correlates of performance monitoring in daily and intermittent smokers. Clin Neurophysiol 125: 1417-1426.
43. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H et al (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27: 2349-2356.
44. Singmann H, Bolker B, Westfall J (2015). afex: Analysis of Factorial Experiments. R package version 0.14-2. http://CRAN.R-project.org/package=afex.
45. Sridharan D, Levitin DJ, Menon V (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci USA 105: 12569-12574.
46. Stoeckel LE, Chai XJ, Zhang J, Whitfield-Gabrieli S, Evins AE (2015). Lower gray matter density and functional connectivity in the anterior insula in smokers compared with never smokers. Addict Biol (e-pub ahead of print; doi:10.1111/adb.12262).
47. Sutherland MT, Carroll AJ, Salmeron BJ, Ross TJ, Hong LE, Stein EA (2013). Down-regulation of amygdala and insula functional circuits by varenicline and nicotine in abstinent cigarette smokers. Biol Psychiatry 74: 538-546.
48. Sutherland MT, McHugh MJ, Pariyadath V, Stein EA (2012). Resting state functional connectivity in addiction: lessons learned and a road ahead. Neuroimage 62: 1-15.
49. Volkow ND, Koob GF, McLellan AT (2016). Neurobiologic advances from the brain disease model of addiction. N Engl J Med 374: 363-371.
50. Wendt M, Luna-Rodriguez A, Jacobsen T (2014). Utility-based early modulation of processing distracting stimulus information. J Neurosci 34: 16720-16725.
51. Xu J, Mendrek A, Cohen MS, Monterosso J, Rodriguez P, Simon SL et al (2005). Brain activity in cigarette smokers performing a working memory task: effect of smoking abstinence. Biol Psychiatry 58: 143-150.
52. Zhang X, Salmeron BJ, Ross TJ, Geng X, Yang Y, Stein EA (2011a). Factors underlying prefrontal and insula structural alterations in smokers. Neuroimage 54: 42-48.
53. Zhang X, Salmeron BJ, Ross TJ, Gu H, Geng X, Yang Y et al (2011b). Anatomical differences and network characteristics underlying smoking cue reactivity. Neuroimage 54: 131-141.