Advertisement

Psychopharmacology

, Volume 228, Issue 1, pp 143–155 | Cite as

Insula’s functional connectivity with ventromedial prefrontal cortex mediates the impact of trait alexithymia on state tobacco craving

  • Matthew T. SutherlandEmail author
  • Allison J. Carroll
  • Betty Jo Salmeron
  • Thomas J. Ross
  • Elliot A. Stein
Original Investigation

Abstract

Rationale

Alexithymia is a personality trait characterized by difficulty indentifying and describing subjective emotional experiences. Decreased aptitude in the perception, evaluation, and communication of affectively laden mental states has been associated with reduced emotion regulation, more severe drug craving in addicts, and structural/functional alterations in insula and anterior cingulate cortex (ACC). The insula and ACC represent sites of convergence between the putative neural substrates of alexithymia and those perpetuating cigarette smoking.

Objectives

We examined the interrelations between alexithymia, tobacco craving, and insula/ACC neurocircuitry using resting-state functional connectivity (rsFC).

Methods

Overnight-deprived smokers (n = 24) and nonsmokers (n = 20) completed six neuroimaging assessments on different days both in the absence of, and following, varenicline and/or nicotine administration. In this secondary analysis of data from a larger study, we assessed trait alexithymia and state tobacco craving using self-reports and examined the rsFC of bilateral insular subregions (anterior, middle, posterior) and dorsal ACC.

Results

Higher alexithymia in smokers predicted reduced rsFC strength between the right anterior insula (aI) and ventromedial prefrontal cortex (vmPFC). Higher alexithymia also predicted more severe tobacco craving during nicotine withdrawal. Critically, the identified aI–vmPFC circuit fully mediated this alexithymia–craving relation. That is, elevated alexithymia predicted decreased aI–vmPFC rsFC and, in turn, decreased aI–vmPFC rsFC predicted increased craving during withdrawal. A moderated mediation analysis indicated that this aI–vmPFC mediational effect was not observed following drug administration.

Conclusions

These results suggest that a weakened right aI–vmPFC functional circuit confers increased liability for tobacco craving during smoking abstinence. Individual differences in alexithymia and/or aI–vmPFC functional coupling may be relevant factors for smoking cessation success.

Keywords

Alexithymia Craving Nicotine Varenicline Resting-state functional connectivity Insula Ventromedial prefrontal cortex fMRI 

Notes

Acknowledgements

This work was sponsored by the National Institute on Drug Abuse Intramural Research Program, National Institutes of Health, Department of Health and Human Services (NIDA-IRP/NIH/DHHS). We thank Eliscia Smith, Angela Neal, Kimberly Slater, Loretta Spurgeon, Anita Signau and the NIDA-IRP nurses, pharmacy, and recruitment staff for assistance with data collection.

Conflicts of interest

The authors declare no conflicts of interest.

Supplementary material

213_2013_3018_MOESM1_ESM.pdf (812 kb)
ESM 1 (PDF 812 KB)

References

  1. Bagby RM, Parker JDA, Taylor GJ (1994) The 20-item Toronto-Alexithymia-Scale: 1. Item selection and cross-validation of the factor structure. J Psychosom Res 38:23–32PubMedCrossRefGoogle Scholar
  2. Baker TB, Piper ME, McCarthy DE, Majeskie MR, Fiore MC (2004) Addiction motivation reformulated: an affective processing model of negative reinforcement. Psychol Rev 111:33–51PubMedCrossRefGoogle Scholar
  3. Baker TB, Piper ME, Schlam TR, Cook JW, Smith SS, Loh WY, Bolt D (2012) Are tobacco dependence and withdrawal related amongst heavy smokers? relevance to conceptualizations of dependence. J Abnorm Psychol 121(4):909-921Google Scholar
  4. Baughman HM, Schwartz S, Schermer JA, Veselka L, Petrides KV, Vernon PA (2011) A Behavioral–genetic study of alexithymia and its relationships with trait emotional intelligence. Twin Res Hum Genet 14:539–543PubMedCrossRefGoogle Scholar
  5. Bechara A, Damasio AR (2005) The somatic marker hypothesis: a neural theory of economic decision. Games Econ Behav 52:336–372CrossRefGoogle Scholar
  6. Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90–101PubMedCrossRefGoogle Scholar
  7. Bibby PA, Ferguson E (2011) The ability to process emotional information predicts loss aversion. Personal Individ Differ 51:263–266CrossRefGoogle Scholar
  8. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Mag Reson Med 34:537–541CrossRefGoogle Scholar
  9. Borsci G, Boccardi M, Rossi R, Rossi G, Perez J, Bonetti M, Frisoni GB (2009) Alexithymia in healthy women: a brain morphology study. J Affect Disord 114:208–215PubMedCrossRefGoogle Scholar
  10. Bruce G, Curren C, Williams L (2012) Alexithymia and alcohol consumption: the mediating effects of drinking motives. Addict Behav 37:350–352PubMedCrossRefGoogle Scholar
  11. Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4:215–222PubMedCrossRefGoogle Scholar
  12. Cauda F, D'Agata F, Sacco K, Duca S, Geminiani G, Vercelli A (2011) Functional connectivity of the insula in the resting brain. Neuroimage 55:8–23PubMedCrossRefGoogle Scholar
  13. Chase HW, Eickhoff SB, Laird AR, Hogarth L (2011) The neural basis of drug stimulus processing and craving: an activation likelihood estimation meta-analysis. Biol Psychiatry 70:785–793PubMedCrossRefGoogle Scholar
  14. Cheetham A, Allen NB, Yucel M, Lubman DI (2010) The role of affective dysregulation in drug addiction. Clin Psychol Rev 30:621–634PubMedCrossRefGoogle Scholar
  15. Chen J, Xu T, Jing J, Chan RC (2011) Alexithymia and emotional regulation: a cluster analytical approach. BMC Psychiatry 11:33. doi: 10.1186/1471-244X-11-33
  16. Cinciripini PM, Tsoh JY, Wetter DW, Lam C, de Moor C, Cinciripini L, Baile W, Anderson C, Minna JD (2005) Combined effects of venlafaxine, nicotine replacement, and brief counseling on smoking cessation. Exp Clin Psychopharmacol 13:282–292PubMedCrossRefGoogle Scholar
  17. Cleland C, Magura S, Foote J, Rosenblum A, Kosanke N (2005) Psychometric properties of the Toronto Alexithymia Scale (TAS-20) for substance users. J Psychosom Res 58:299–306PubMedCrossRefGoogle Scholar
  18. Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666PubMedGoogle Scholar
  19. Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9:566–571PubMedCrossRefGoogle Scholar
  20. Craig AD (2009) How do you feel — now? The anterior insula and human awareness. Nature Rev Neurosci 10:59–70CrossRefGoogle Scholar
  21. Craig AD (2010) The sentient self. Brain Struct Funct 214:563–577PubMedCrossRefGoogle Scholar
  22. Cravello L, Caltagirone C, Spalletta G (2009) The SNRI venlafaxine improves emotional unawareness in patients with post-stroke depression. Hum Psychopharmacol Clin Exp 24:331–336CrossRefGoogle Scholar
  23. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nature Neurosci 7:189–195PubMedCrossRefGoogle Scholar
  24. de Timary P, Luts A, Hers D, Luminet O (2008) Absolute and relative stability of alexithymia in alcoholic inpatients undergoing alcohol withdrawal: relationship to depression and anxiety. Psychiatry Res 157:105–113PubMedCrossRefGoogle Scholar
  25. Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21:1498–1506PubMedCrossRefGoogle Scholar
  26. Dosenbach NUF, Visscher KM, Palmer ED, Miezin FM, Wenger KK, Kang HSC, Burgund ED, Grimes AL, Schlaggar BL, Petersen SE (2006) A core system for the implementation of task sets. Neuron 50:799–812PubMedCrossRefGoogle Scholar
  27. Engelmann JM, Versace F, Robinson JD, Minnix JA, Lam CY, Cui Y, Brown VL, Cinciripini PM (2012) Neural substrates of smoking cue reactivity: a meta-analysis of fMRI studies. Neuroimage 60:252–262PubMedCrossRefGoogle Scholar
  28. Ferguson E, Bibby PA, Rosamond S, O'Grady C, Parcell A, Amos C, McCutcheon C, O'Carroll R (2009) Alexithymia, cumulative feedback, and differential response patterns on the Iowa Gambling Task. J Personal 77:883–902CrossRefGoogle Scholar
  29. Ferguson SG, Shiffman S (2009) The relevance and treatment of cue-induced cravings in tobacco dependence. J Subst Abus Treat 36:235–243CrossRefGoogle Scholar
  30. Foland-Ross LC, Altshuler LL, Bookheimer SY, Lieberman MD, Townsend J, Penfold C, Moody T, Ahlf K, Shen JK, Madsen SK, Rasser PE, Toga AW, Thompson PM (2010) Amygdala reactivity in healthy adults is correlated with prefrontal cortical thickness. J Neurosci 30:16673–16678PubMedCrossRefGoogle Scholar
  31. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711PubMedCrossRefGoogle Scholar
  32. Franklin T, Wang Z, Suh JJ, Hazan R, Cruz J, Li Y, Goldman M, Detre JA, O'Brien CP, Childress AR (2011) Effects of varenicline on smoking cue-triggered neural and craving responses. Arch Gen Psychiat 68:516–526PubMedCrossRefGoogle Scholar
  33. Frewen PA, Lanius RA, Dozois DJA, Neufeld RWJ, Pain C, Hopper JW, Densmore M, Stevens TK (2008) Clinical and neural correlates of alexithymia in posttraumatic stress disorder. J Abnorm Psychol 117:171–181PubMedCrossRefGoogle Scholar
  34. Goldstein RZ, Craig AD, Bechara A, Garavan H, Childress AR, Paulus MP, Volkow ND (2009) The neurocircuitry of impaired insight in drug addiction. Trends Cogn Sci 13:372–380PubMedCrossRefGoogle Scholar
  35. Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78PubMedCrossRefGoogle Scholar
  36. Hare TA, Camerer CF, Rangel A (2009) Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324:646–648PubMedCrossRefGoogle Scholar
  37. Heinzel A, Schafer R, Muller HW, Schieffer A, Ingenhag A, Northoff G, Franz M, Hautzel H (2010) Differential modulation of valence and arousal in high-alexithymic and low-alexithymic individuals. Neuroreport 21:998–1002PubMedGoogle Scholar
  38. Heishman SJ, Singleton EG, Pickworth WB (2008) Reliability and validity of a short form of the tobacco craving questionnaire. Nicotine Tob Res 10:643–651PubMedCrossRefGoogle Scholar
  39. Herbert BM, Herbert C, Pollatos O (2011) On the relationship between interoceptive awareness and alexithymia: is interoceptive awareness related to emotional awareness? J Personal 79:1149–1175CrossRefGoogle Scholar
  40. Hong LE, Gu H, Yang Y, Ross TJ, Salmeron BJ, Buchholz B, Thaker GK, Stein EA (2009) Association of nicotine addiction and nicotine's actions with separate cingulate cortex functional circuits. Arch Gen Psychiatry 66:431–441PubMedCrossRefGoogle Scholar
  41. Janes AC, Pizzagalli DA, Richardt S, Frederick BD, Chuzi S, Pachas G, Culhane MA, Holmes AJ, Fava M, Evins AE, Kaufman MJ (2010) Brain reactivity to smoking cues prior to smoking cessation predicts ability to maintain tobacco abstinence. Biol Psychiatry 67:722–729PubMedCrossRefGoogle Scholar
  42. Junghanns K, Tietz U, Dibbelt L, Kuether M, Jurth R, Ehrenthal D, Blank S, Backhaus J (2005) Attenuated salivary cortisol secretion under cue exposure is associated with early relapse. Alcohol Alcohol 40:80–85PubMedCrossRefGoogle Scholar
  43. Kable JW, Glimcher PW (2009) The neurobiology of decision: consensus and controversy. Neuron 63:733–745PubMedCrossRefGoogle Scholar
  44. Kano M, Fukudo S, Gyoba J, Kamachi M, Tagawa M, Mochizuki H, Itoh M, Hongo M, Yanai K (2003) Specific brain processing of facial expressions in people with alexithymia: an (H2O)-O-15-PET study. Brain 126:1474–1484PubMedCrossRefGoogle Scholar
  45. Kano M, Hamaguchi T, Itoh M, Yanai K, Fukudo S (2007) Correlation between alexithymia and hypersensitivity to visceral stimulation in human. Pain 132:252–263PubMedCrossRefGoogle Scholar
  46. Kano M, Ito M, Fukudo S (2011) Neural substrates of decision making as measured with the Iowa Gambling Task in men with alexithymia. Psychosom Med 73:588–597PubMedCrossRefGoogle Scholar
  47. Kano M, Mizuno T, Kawano Y, Aoki M, Kanazawa M, Fukudo S (2012) Serotonin transporter gene promoter polymorphism and alexithymia. Neuropsychobiology 65:76–82PubMedCrossRefGoogle Scholar
  48. Keller DS, Carroll KM, Nich C, Rounsaville BJ (1995) Alexithymia in cocaine abusers — response to psychotherapy and pharmacotherapy. Am J Addict 4:234–244CrossRefGoogle Scholar
  49. Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, Marchante AN, Whalen PJ (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223:403–410PubMedCrossRefGoogle Scholar
  50. Kober H, Mende-Siedlecki P, Kross EF, Weber J, Mischel W, Hart CL, Ochsner KN (2010) Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc Natl Acad Sci U S A 107:14811–14816PubMedCrossRefGoogle Scholar
  51. Kuhn S, Schubert F, Gallinat J (2010) Reduced thickness of medial orbitofrontal cortex in smokers. Biol Psychiatry 68:1061–1065PubMedCrossRefGoogle Scholar
  52. Kun B, Demetrovics Z (2010) Emotional intelligence and addictions: a systematic review. Subst Use Misuse 45:1131–1160PubMedCrossRefGoogle Scholar
  53. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534PubMedCrossRefGoogle Scholar
  54. Li CSR, Sinha R (2006) Alexithymia and stress-induced brain activation in cocaine-dependent men and women. J Psychiatry Neurosci 31:115–121PubMedGoogle Scholar
  55. Lieberman MD, Eisenberger NI, Crockett MJ, Tom SM, Pfeifer JH, Way BM (2007) Putting feelings into words — affect labeling disrupts amygdala activity in response to affective stimuli. Psychol Sci 18:421–428PubMedCrossRefGoogle Scholar
  56. Loas G, Fremaux D, Boyer P (1997a) Anhedonia and alexithymia: distinct or overlapping constructs. Percept Mot Skills 84:415–425PubMedCrossRefGoogle Scholar
  57. Loas G, Fremaux D, Otmani O, Lecercle C, Delahousse J (1997b) Is alexithymia a negative factor for maintaining abstinence? A follow-up study. Compr Psychiatry 38:296–299PubMedCrossRefGoogle Scholar
  58. Mattila AK, Keefer KV, Taylor GJ, Joukamaa M, Jula A, Parker JDA, Bagby RM (2010) Taxometric analysis of alexithymia in a general population sample from Finland. Pers Individ Differ 49:216–221CrossRefGoogle Scholar
  59. Meriau K, Wartenburger I, Kazzer P, Prehn K, Lammers CH, van der Meer E, Villringer A, Heekeren HR (2006) A neural network reflecting individual differences in cognitive processing of emotions during perceptual decision making. Neuroimage 33:1016–1027PubMedCrossRefGoogle Scholar
  60. Miyake Y, Okamoto Y, Onoda K, Shirao N, Okamoto Y, Yamawaki S (2012) Brain activation during the perception of stressful word stimuli concerning interpersonal relationships in anorexia nervosa patients with high degrees of alexithymia in an fMRI paradigm. Psychiatry Res-Neuroimaging 201:113–119CrossRefGoogle Scholar
  61. Moriguchi Y, Decety J, Ohnishi T, Maeda M, Mori T, Nemoto K, Matsuda H, Komaki G (2007) Empathy and judging other's pain: an fMRI study of alexithymia. Cereb Cortex 17:2223–2234PubMedCrossRefGoogle Scholar
  62. Myers-Schulz B, Koenigs M (2012) Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Mol Psychiatry 17:132–141PubMedCrossRefGoogle Scholar
  63. Naqvi NH, Bechara A (2010) The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making. Brain Struct Funct 214:435–450PubMedCrossRefGoogle Scholar
  64. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531–534PubMedCrossRefGoogle Scholar
  65. Nieuwenhuys R (2012) The insular cortex: a review. Prog Brain Res 195:123–163PubMedCrossRefGoogle Scholar
  66. Ochsner KN, Gross JJ (2005) The cognitive control of emotion. Trends Cogn Sci 9:242–249PubMedCrossRefGoogle Scholar
  67. Ogrodniczuk JS, Piper WE, Joyce AS (2011) Effect of alexithymia on the process and outcome of psychotherapy: a programmatic review. Psychiatry Res 190:43–48PubMedCrossRefGoogle Scholar
  68. Paradiso S, Vaidya JG, McCormick LM, Jones A, Robinson RG (2008) Aging and alexithymia: association with reduced right rostral cingulate volume. Am J Geriatr Psychiatry 16:760–769PubMedCrossRefGoogle Scholar
  69. Parker JD, Keefer KV, Taylor GJ, Bagby RM (2008) Latent structure of the alexithymia construct: a taxometric investigation. Psychol Assess 20:385–396PubMedCrossRefGoogle Scholar
  70. Payer DE, Lieberman MD, London ED (2012) Neural correlates of affect processing and aggression in methamphetamine dependence. Arch Gen Psychiatry 68:271–282CrossRefGoogle Scholar
  71. Pollatos O, Gramann K (2012) Attenuated modulation of brain activity accompanies emotion regulation deficits in alexithymia. Psychophysiology 49:651–658PubMedCrossRefGoogle Scholar
  72. Pouga L, Berthoz S, de Gelder B, Grezes J (2010) Individual differences in socioaffective skills influence the neural bases of fear processing: the case of alexithymia. Hum Brain Mapp 31:1469–1481PubMedCrossRefGoogle Scholar
  73. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154PubMedCrossRefGoogle Scholar
  74. Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40:879–891PubMedCrossRefGoogle Scholar
  75. Preacher KJ, Rucker DD, Hayes AF (2007) Addressing moderated mediation hypotheses: theory, methods, and prescriptions. Multivar Behav Res 42:185–227CrossRefGoogle Scholar
  76. Prince JD, Berenbaum H (1993) Alexithymia and hedonic capacity. J Res Pers 27:15–22CrossRefGoogle Scholar
  77. Reker M, Ohrmann P, Rauch AV, Kugel H, Bauer J, Dannlowski U, Arolt V, Heindel W, Suslow T (2010) Individual differences in alexithymia and brain response to masked emotion faces. Cortex 46:658–667PubMedCrossRefGoogle Scholar
  78. Saladin ME, Santa Ana EJ, LaRowe SD, Simpson AN, Tolliver BK, Price KL, McRae-Clark AL, Brady KT (2012) Does alexithymia explain variation in cue-elicited craving reported by methamphetamine-dependent individuals? Am J Addict 21:130–135PubMedCrossRefGoogle Scholar
  79. Satterthwaite TD, Wolf DH, Loughead J, Ruparel K, Elliott MA, Hakonarson H, Gur RC, Gur RE (2012) Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. Neuroimage 60:623–632PubMedCrossRefGoogle Scholar
  80. Shiffman S, Engberg JB, Paty JA, Perz WG, Gnys M, Kassel JD, Hickcox M (1997) A Day at a time: predicting smoking lapse from daily urge. J Abnorm Psychol 106:104–116PubMedCrossRefGoogle Scholar
  81. Silani G, Bird G, Brindley R, Singer T, Frith C, Frith U (2008) Levels of emotional awareness and autism: an fMRI study. Soc Neurosci 3:97–112PubMedCrossRefGoogle Scholar
  82. Speranza M, Corcos M, Stephan P, Loas G, Perez-Diaz F, Lang F, Venisse JL, Bizouard P, Flament M, Halfon O, Jeammet P (2004) Alexithymia, depressive experiences, and dependency in addictive disorders. Subst Use Misuse 39:551–579PubMedCrossRefGoogle Scholar
  83. Subcommittee SRNT (2002) Biochemical verification of tobacco use and cessation. Nic Tob Res 4:149–159CrossRefGoogle Scholar
  84. Stasiewicz PR, Bradizza CM, Gudleski GD, Coffey SF, Schlauch RC, Bailey ST, Bole CW, Gulliver SB (2012) The relationship of alexithymia to emotional dysregulation within an alcohol dependent treatment sample. Addict Behav 37:469–476PubMedCrossRefGoogle Scholar
  85. Sutherland MT, Carroll AJ, Salmeron BJ, Ross TJ, Hong LE, Stein EA (2013a) Down-regulation of amygdala and insula functional circuits in abstinent cigarette smokers by varenicline and nicotine. Bio Psychiatry. doi: 10.1016/j.biopsych.2013.01.035
  86. Sutherland MT, Carroll AJ, Salmeron BJ, Ross TJ, Hong LE, Stein EA (2013b) Individual differences in amygdala reactivity following nicotinic receptor engagement in abstinent smokers. Neuroimage. doi: 10.1016/j.neuroimage.2012.10.043
  87. Sutherland MT, McHugh M, Pariyadath V, Stein EA (2013c) Resting state functional connectivity in addiction: lessons learned and a road ahead. Neuroimage. doi: 10.1016/j.neuroimage.2012.01.117
  88. Swart M, Bruggeman R, Laroi F, Alizadeh BZ, Kema I, Kortekaas R, Wiersma D, Aleman A (2011) COMT Val158Met polymorphism, verbalizing of emotion and activation of affective brain systems. Neuroimage 55:338–344PubMedCrossRefGoogle Scholar
  89. Swart M, Kortekaas R, Aleman A (2009) Dealing with feelings: characterization of trait alexithymia on emotion regulation strategies and cognitive-emotional processing. PLoS One 4.Google Scholar
  90. Takeuchi H, Taki Y, Sassa Y, Hashizume H, Sekiguchi A, Fukushima A, Kawashima R (2011) Regional gray matter density associated with emotional intelligence: evidence from voxel-based morphometry. Hum Brain Mapp 32:1497–1510PubMedCrossRefGoogle Scholar
  91. Taylor GJ (2000) Recent developments in alexithymia theory and research. Can J Psychiatry-Rev Can Psychiatr 45:134–142Google Scholar
  92. Taylor GJ, Bagby RM (2004) New trends in alexithymia research. Psychother Psychosom 73:68–77PubMedCrossRefGoogle Scholar
  93. Taylor KS, Seminowicz DA, Davis KD (2009) Two systems of resting state connectivity between the insula and cingulate cortex. Hum Brain Mapp 30:2731–2745PubMedCrossRefGoogle Scholar
  94. Thorberg FA, Young RM, Sullivan KA, Lyvers M (2009) Alexithymia and alcohol use disorders: a critical review. Addict Behav 34:237–245PubMedCrossRefGoogle Scholar
  95. Thorberg FA, Young RM, Sullivan KA, Lyvers M, Connor JP, Feeney GFX (2011) Alexithymia, craving and attachment in a heavy drinking population. Addict Behav 36:427–430PubMedCrossRefGoogle Scholar
  96. Tolmunen T, Heliste M, Lehto SM, Hintikka J, Honkalampi K, Kauhanen J (2011) Stability of alexithymia in the general population: an 11-year follow-up. Compr Psychiatry 52:536–541PubMedCrossRefGoogle Scholar
  97. Verdejo-Garcia A, Clark L, Dunn BD (2012) The role of interoception in addiction: a critical review. Neurosci Biobehav Rev 36:1857–1869PubMedCrossRefGoogle Scholar
  98. Wang Z, Faith M, Patterson F, Tang K, Kerrin K, Wileyto EP, Detre JA, Lerman C (2007) Neural substrates of abstinence-induced cigarette cravings in chronic smokers. J Neurosci 27:14035–14040PubMedCrossRefGoogle Scholar
  99. Watson D, Clark LA, Tellegen A (1988) Development and validation of brief measures of positive and negative affect: the PANAS Scales. J Pers Soc Psych 54:1063–1070CrossRefGoogle Scholar
  100. Wingbermuhle E, Theunissen H, Verhoeven WMA, Kessels RPC, Egger JIM (2012) The neurocognition of alexithymia: evidence from neuropsychological and neuroimaging studies. Acta Neuropsychiatrica 24:67–80CrossRefGoogle Scholar
  101. Zhang X, Salmeron BJ, Ross TJ, Geng X, Yang Y, Stein EA (2011) Factors underlying prefrontal and insula structural alterations in smokers. Neuroimage 54:42–48PubMedCrossRefGoogle Scholar
  102. Ziolkowski M, Gruss T, Rybakowski JK (1995) Does alexithymia in male alcoholics constitute a negative factor for maintaining abstinence. Psychother Psychosom 63:169–173PubMedCrossRefGoogle Scholar
  103. Zubieta JK, Heitzeg MM, Xu YJ, Koeppe RA, Ni LS, Guthrie S, Domino EF (2005) Regional cerebral blood flow responses to smoking in tobacco smokers after overnight abstinence. Am J Psychiat 162:567–577PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2013

Authors and Affiliations

  • Matthew T. Sutherland
    • 1
    • 2
    • 3
    Email author
  • Allison J. Carroll
    • 2
  • Betty Jo Salmeron
    • 2
  • Thomas J. Ross
    • 2
  • Elliot A. Stein
    • 2
  1. 1.Department of PsychologyFlorida International UniversityMiamiUSA
  2. 2.Neuroimaging Research Branch, National Institute on Drug Abuse, Intramural Research Program, NIH/DHHSBaltimoreUSA
  3. 3.Department of PsychologyFlorida International University, Deuxieme MaisonMiamiUSA

Personalised recommendations