Aberrant network integrity of the inferior frontal cortex in women with anorexia nervosa

NeuroImage: Clinical

Volumn 4, Issue , 2014, Pages 615-622

  Kullmann, Stephanie ^a,b,c   Giel, Katrin E ^c   Teufel, Martin ^c   Thiel, Ansgar ^c   Zipfel, Stephan ^a   Preissl, Hubert ^a,b,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Anorexia nervosa; Effective connectivity; Functional connectivity; Resting state fMRI

Indexed keywords

ADULT; ANOREXIA NERVOSA; ARTICLE; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; EXECUTIVE FUNCTION; FEMALE; FRONTAL CORTEX; FRONTAL GYRUS; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; ORBITOFRONTAL GYRUS; PHYSICAL ACTIVITY; PRIORITY JOURNAL; ASSESSMENT OF HUMANS; ATHLETE; CINGULATE GYRUS; DEPRESSION SUM SCORE; EATING DISORDER INVENTORY; EFFECTIVE CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MIDCINGULUM; ORBITAL CORTEX; RESTING STATE NETWORK; SCORING SYSTEM; STATE ANXIETY SCORE; ADOLESCENT; ANALYSIS OF VARIANCE; BLOOD; CASE CONTROL STUDY; FRONTAL LOBE; IMAGE PROCESSING; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; REST; SELF REPORT; STATISTICS; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ANOREXIA NERVOSA; CASE-CONTROL STUDIES; FEMALE; FRONTAL LOBE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; NERVE NET; OXYGEN; REST; SELF REPORT; STATISTICS AS TOPIC; YOUNG ADULT;

EID: 84898603135     PISSN: None     EISSN: 22131582     Source Type: Journal    
DOI: 10.1016/j.nicl.2014.04.002     Document Type: Article

References (79)

1. Diagnostic and Statistical Manual of Mental Disorders, 4th ed., Text Revision (DSM-IV-TR). Washington, DC. American Psychiatric Association.
2. Asahi S., Okamoto Y., Okada G., Yamawaki S., Yokota N. Negative correlation between right prefrontal activity during response inhibition and impulsiveness: a fMRI study European Archi (Pubitemid 39312839)
3. Brewerton T.D., Stellefson E.J., Hibbs N., Hodges E.L., Cochrane C.E. Comparison of eating disorder patients with and without compulsive exercising International Journal of Eating Disorders 17 1995 413 416 10.1002/1098- 108X(199505)17:4<413::AID-EAT2260170414>3.0.CO;2-0 7620482
4. Brooks S.J., O'Daly O., Uher R., Friederich H.C., Giampietro V., Brammer M., Williams S.C., Schioth H.B., Treasure J., Campbell I.C. Thinking about eating food activates visual cortex with reduced bilateral cerebellar activation in females with anorexia nervosa: an fMRI study PloS One 7 2012 e34000 10.1371/journal.pone.0034000 22479499
5. Brooks S.J., O'Daly O.G., Uher R., Friederich H.C., Giampietro V., Brammer M., Williams S.C., Schioth H.B., Treasure J., Campbell I.C. Differential neural responses to food images in women with bulimia versus anorexia nervosa PloS One 6 2011 e22259 10.1371/journal.pone.0022259 21799807
6. Brooks S.J., Rask-Andersen M., Benedict C., Schioth H.B. A debate on current eating disorder diagnoses in light of neurobiological findings: is it time for a spectrum model? BMC Psychiatry 12 2012 76
7. Bruch H Perceptual and conceptual disturbances in anorexia nervosa Psychosomatic Medicine 24 1962 187 194 13873828
8. Buckner R.L., Sepulcre J., Talukdar T., Krienen F.M., Liu H., Hedden T., Andrews-Hanna J.R., Sperling R.A., Johnson K.A. Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease Journal of Neuroscience: the Official Journal of the Society for Neuroscience 29 2009 1860 1873 10.1523/JNEUROSCI.5062-08.2009 19211893
9. Bullmore E., Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems Journal of Neuroscience: the Official Journal of the Society for Neuroscience 10 2009 186 198 19190637
10. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex Trends in Cognitive Sciences 4 2000 215 222 10.1016/S1364-6613(00)01483-2 10827444 (Pubitemid 30332147)
11. Carrera O., Adan R.A., Gutierrez E., Danner U.N., Hoek H.W., van Elburg A.A., Kas M.J. Hyperactivity in anorexia nervosa: warming up not just burning-off calories PloS One 7 2012 e41851 10.1371/journal.pone.0041851 22848634
12. Carter J.C., Blackmore E., Sutandar-Pinnock K., Woodside D.B. Relapse in anorexia nervosa: a survival analysis Psychological Medicine 34 2004 671 679 10.1017/S0033291703001168 15099421 (Pubitemid 38735461)
13. Casper R.C., Jasbine L.N. An eight-year follow-up: outcome from adolescent compared to adult onset anorexia nervosa Journal of Youth and Adolescence 25 1996 499 517 10.1007/BF01537545 (Pubitemid 126327750)
14. Chao-Gan Y., Yu-Feng Z. DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state fMRI Frontiers in Systems Neuroscience 4 2010 13 20577591
15. Cole D.M., Smith S.M., Beckmann C.F. Advances and pitfalls in the analysis and interpretation of resting-state FMRI data Frontiers in Systems Neuroscience 4 2010 8 20407579
16. Cowdrey F.A., Filippini N., Park R.J., Smith S.M., McCabe C. Increased resting state functional connectivity in the default mode network in recovered anorexia nervosa Human Brain Mapping 2014 23033154
17. Critchley H.D Neural mechanisms of autonomic, affective, and cognitive integration Journal of Comparative Neurology 493 2005 154 166 10.1002/cne.20749 16254997 (Pubitemid 41636198)
18. Davis C., Blackmore E., Katzman D.K., Fox J. Female adolescents with anorexia nervosa and their parents: a case-control study of exercise attitudes and behaviours Psychological Medicine 35 2005 377 386 10.1017/S0033291704003447 15841873 (Pubitemid 40372476)
19. Davis C., Brewer H., Ratusny D. Behavioral frequency and psychological commitment: necessary concepts in the study of excessive exercising Journal of Behavioral Medicine 16 1993 611 628 10.1007/BF00844722 8126715 (Pubitemid 24012917)
20. Ding L., Worrell G.A., Lagerlund T.D., He B. Spatio-temporal source localization and Granger causality in ictal source analysis Conference Proceedings:. Annual International Conference of the IEEE Engineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Conference 1 2006 3670 3671 17947049 (Pubitemid 46520706)
21. 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 Proceedings of the National Academy of Sciences of the United States of America 104 2007 11073 11078 10.1073/pnas.0704320104 17576922 (Pubitemid 47175228)
22. 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 50 2006 799 812 10.1016/j.neuron.2006.04.031 16731517 (Pubitemid 43775735)
23. Duann J.R., Ide J.S., Luo X., Li C.S. Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition Journal of Neuroscience: the Official Journal of the Society for Neuroscience 29 2009 10171 10179 10.1523/JNEUROSCI.1300-09.2009 19675251
24. Fairburn C.G., Cooper Z. The Eating Disorder Examination twelfth edition C.G. Fairburn G.T. Wilson Binge Eating: Nature Assessment and Treatment 1993 Guilford Publications New York 317 360
25. Favaro A., Santonastaso P., Manara R., Bosello R., Bommarito G., Tenconi E., Di Salle F. Disruption of visuospatial and somatosensory functional connectivity in anorexia nervosa Biological Psychiatry 72 2012 864 870 10.1016/j.biopsych.2012.04.025 22633945
26. Fessler D.M Pseudoparadoxical impulsivity in restrictive anorexia nervosa: a consequence of the logic of scarcity International Journal of Eating Disorders 31 2002 376 388 10.1002/eat.10035 11948643 (Pubitemid 34275047)
27. Fladung A.K., Gron G., Grammer K., Herrnberger B., Schilly E., Grasteit S., Wolf R.C., Walter H., von Wietersheim J. A neural signature of anorexia nervosa in the ventral striatal reward system American Journal of Psychiatry 167 2010 206 212 10.1176/appi.ajp.2009.09010071 19833790
28. Frank G.K., Bailer U.F., Henry S.E., Drevets W., Meltzer C.C., Price J.C., Mathis C.A., Wagner A., Hoge J., Ziolko S., Barbarich-Marsteller N., Weissfeld L., Kaye W.H. Increased dopamine D2/D3 receptor binding after recovery from anorexia nervosa measured by positron emission tomography and [11c]raclopride Biological Psychiatry 58 2005 908 912 10.1016/j.biopsych.2005. 05.003 15992780 (Pubitemid 41790720)
29. Frank G.K., Reynolds J.R., Shott M.E., Jappe L., Yang T.T., Tregellas J.R., O'Reilly R.C. Anorexia nervosa and obesity are associated with opposite brain reward response Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 37 2012 2031 2046 10.1038/npp.2012.51 22549118
30. Frank S., Kullmann S., Veit R. Food related processes in the insular cortex Frontiers in Human Neuroscience 7 2013 499 23986683
31. Garcia-Garcia I., Jurado M.A., Garolera M., Segura B., Sala-Llonch R., Marques-Iturria I., Pueyo R., Sender-Palacios M.J., Vernet-Vernet M., Narberhaus A., Ariza M., Junque C. Alterations of the salience network in obesity: a resting-state fMRI study Human Brain Mapping 2012
32. Garner D.M Eating Disorder Inventory - 2: Professional Manual 1991 Psychological Assessment Resources
33. Giel K.E., Kullmann S., Preissl H., Bischoff S.C., Thiel A., Schmidt U., Zipfel S., Teufel M. Understanding the reward system functioning in anorexia nervosa: crucial role of physical activity Biological Psychology 94 2013 575 581 10.1016/j.biopsycho.2013.10.004 24161801
34. Granger C Investigating causal relations by econometric models and cross-spectral methods Econometrica 37 1969 424 438 10.2307/1912791
35. Gray J.A The psychophysiological basis of introversion-extraversion Behaviour Research and Therapy 8 1970 249 266 10.1016/0005-7967(70)90069-0 5470377
36. Greicius M.D., Flores B.H., Menon V., Glover G.H., Solvason H.B., Kenna H., Reiss A.L., Schatzberg A.F. Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus Biological Psychiatry 62 2007 429 437 10.1016/j.biopsych.2006.09. 020 17210143 (Pubitemid 47284017)
37. Greicius M.D., Srivastava G., Reiss A.L., Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI Proceedings of the National Academy of Sciences of the United States of America 101 2004 4637 4642 10.1073/pnas.0308627101 15070770 (Pubitemid 38437463)
38. Hebebrand J., Bulik C.M. Critical appraisal of the provisional DSM-5 criteria for anorexia nervosa and an alternative proposal International Journal of Eating Disorders 44 2011 665 678 10.1002/eat.20875 22072403
39. Jiao Q., Lu G., Zhang Z., Zhong Y., Wang Z., Guo Y., Li K., Ding M., Liu Y. Granger causal influence predicts BOLD activity levels in the default mode network Human Brain Mapping 32 2011 154 161 10.1002/hbm.21065 21157880
40. Kaye W.H., Fudge J.L., Paulus M. New insights into symptoms and neurocircuit function of anorexia nervosa Nature Reviews Neuroscience 10 2009 573 584 10.1038/nrn2682
41. Kaye W.H., Wierenga C.E., Bailer U.F., Simmons A.N., Bischoff-Grethe A. Nothing tastes as good as skinny feels: the neurobiology of anorexia nervosa Trends in Neurosciences 36 2013 110 120 10.1016/j.tins.2013.01.003 23333342
42. Keating C., Tilbrook A.J., Rossell S.L., Enticott P.G., Fitzgerald P.B. Reward processing in anorexia nervosa Neuropsychologia 50 2012 567 575 10.1016/j.neuropsychologia.2012.01.036 22349445
43. Kim K.R., Ku J., Lee J.H., Lee H., Jung Y.C. Functional and effective connectivity of anterior insula in anorexia nervosa and bulimia nervosa Neuroscience Letters 521 2012 152 157 10.1016/j.neulet.2012.05.075 22684096
44. Kullmann S., Giel K.E., Hu X., Bischoff S.C., Teufel M., Thiel A., Zipfel S., Preissl H. Impaired inhibitory control in anorexia nervosa elicited by physical activity stimuli Social Cognitive and Affective Neuroscience 2013 23677490
45. Kullmann S., Heni M., Veit R., Ketterer C., Schick F., Haring H.U., Fritsche A., Preissl H. The obese brain: association of body mass index and insulin sensitivity with resting state network functional connectivity Human Brain Mapping 33 2012 1052 1061 10.1002/hbm.21268 21520345
46. Kullmann S., Pape A.A., Heni M., Ketterer C., Schick F., Haring H.U., Fritsche A., Preissl H., Veit R. Functional network connectivity underlying food processing: disturbed salience and visual processing in overweight and obese adults Cerebral Cortex (New York, N.Y.: 1991) 23 2013 1247 1256 10.1093/cercor/bhs124 22586138
47. Lock J., Garrett A., Beenhakker J., Reiss A.L. Aberrant brain activation during a response inhibition task in adolescent eating disorder subtypes American Journal of Psychiatry 168 2011 55 64 10.1176/appi.ajp.2010.10010056 21123315
48. McFadden K.L., Tregellas J.R., Shott M.E., Frank G.K. Reduced salience and default mode network activity in women with anorexia nervosa Journal of Psychiatry and Neuroscience 38 2013 130046 24280181
49. Meda S.A., Stevens M.C., Folley B.S., Calhoun V.D., Pearlson G.D. Evidence for anomalous network connectivity during working memory encoding in schizophrenia: an ICA based analysis PloS One 4 2009 e7911 10.1371/journal.pone. 0007911 19936244
50. Nunn K., Frampton I., Gordon I., Lask B. The fault is not in her parents but in her insula - a neurobiological hypothesis of anorexia nervosa European Eating Disorders Review: the Journal of the Eating Disorders Association 16 2008 355 360 10.1002/erv.890 18711713
51. Oberndorfer T.A., Kaye W.H., Simmons A.N., Strigo I.A., Matthews S.C. Demand-specific alteration of medial prefrontal cortex response during an inhibition task in recovered anorexic women International Journal of Eating Disorders 44 2011 1 8 10.1002/eat.20750 20127942
52. Paul T., Thiel A. EDI-2. Eating Disorder Inventory - 2 Deutsche Version 2005 Hogrefe Göttingen, Germany
53. Penas-Lledo E., Vaz Leal F.J., Waller G. Excessive exercise in anorexia nervosa and bulimia nervosa: relation to eating characteristics and general psychopathology International Journal of Eating Disorders 31 2002 370 375 10.1002/eat.10042 11948642 (Pubitemid 34275046)
54. Pietrini F., Castellini G., Ricca V., Polito C., Pupi A., Faravelli C. Functional neuroimaging in anorexia nervosa: a clinical approach European Psychiatry: the Journal of the Association of European Psychiatrists 26 2011 176 182 10.1016/j.eurpsy.2010.07.011 20934859
55. Qi R., Zhang L.J., Zhong J., Zhang Z., Ni L., Jiao Q., Liao W., Zheng G., Lu G. Altered effective connectivity network of the basal ganglia in low-grade hepatic encephalopathy: a resting-state fMRI study with Granger causality analysis PloS One 8 2013 e53677 10.1371/journal.pone.0053677 23326484
56. Rolls E.T Taste, olfactory, and food texture processing in the brain, and the control of food intake Physiology & Behavior 85 2005 45 56 10.1016/j.physbeh.2005.04.012 15924905 (Pubitemid 40744975)
57. Rolls E.T., Yaxley S., Sienkiewicz Z.J. Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey Journal of Neurophysiology 64 1990 1055 1066 2258734 (Pubitemid 20338951)
58. Scheurink A.J., Boersma G.J., Nergardh R., Sodersten P. Neurobiology of hyperactivity and reward: agreeable restlessness in anorexia nervosa Physiology & Behavior 100 2010 490 495 10.1016/j.physbeh.2010.03.016 20361989
59. 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 Journal of Neuroscience: the Official Journal of the Society for Neuroscience 27 2007 2349 2356 10.1523/JNEUROSCI. 5587-06.2007 17329432 (Pubitemid 46340968)
60. Song X.W., Dong Z.Y., Long X.Y., Li S.F., Zuo X.N., Zhu C.Z., He Y., Yan C.G., Zang Y.F. REST: a toolkit for resting-state functional magnetic resonance imaging data processing PloS One 6 2011 e25031 10.1371/journal.pone.0025031 21949842
61. Stephan K.E., Roebroeck A. A short history of causal modeling of fMRI data Neuroimage 62 2012 856 863 10.1016/j.neuroimage.2012.01.034 22248576
62. Strobel A., Beauducel A., Debener S., Brocke B. Eine deutschsprachige Version des BIS/BAS-Fragebogens von Carver und White Zeitschrift Für Differentielle und Diagnostische Psychologie 22 2001 216 227 10.1024//0170-1789.22.3.216 (Pubitemid 33352366)
63. Strober M., Freeman R., Morrell W. The long-term course of severe anorexia nervosa in adolescents: survival analysis of recovery, relapse, and outcome predictors over 10-15 years in a prospective study International Journal of Eating Disorders 22 1997 339 360 10.1002/(SICI)1098-108X(199712)22:4<339: :AID-EAT1>3.0.CO;2-N 9356884 (Pubitemid 27459516)
64. Tchanturia K., Anderluh M.B., Morris R.G., Rabe-Hesketh S., Collier D.A., Sanchez P., Treasure J.L. Cognitive flexibility in anorexia nervosa and bulimia nervosa Journal of the International Neuropsychological Society: JINS 10 2004 513 520 10.1017/S1355617704104086 15327730 (Pubitemid 39077192)
65. Torta D.M., Cauda F. Different functions in the cingulate cortex, a meta-analytic connectivity modeling study Neuroimage 56 2011 2157 2172 10.1016/j.neuroimage.2011.03.066 21459151
66. Uddin L.Q., Kelly A.M., Biswal B.B., Castellanos F.X., Milham M.P. Functional connectivity of default mode network components: correlation, anticorrelation, and causality Human Brain Mapping 30 2009 625 637 10.1002/hbm.20531 18219617
67. Uher R., Murphy T., Brammer M.J., Dalgleish T., Phillips M.L., Ng V.W., Andrew C.M., Williams S.C., Campbell I.C., Treasure J. Medial prefrontal cortex activity associated with symptom provocation in eating disorders American Journal of Psychiatry 161 2004 1238 1246 10.1176/appi.ajp.161.7.1238 15229057 (Pubitemid 38859174)
68. Vitousek K., Manke F. Personality variables and disorders in anorexia nervosa and bulimia nervosa Journal of Abnormal Psychology 103 1994 137 147 10.1037/0021-843X.103.1.137 8040475 (Pubitemid 24066963)
69. Vogt B.A., Finch D.M., Olson C.R. Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions Cerebral Cortex (New York, N.Y.: 1991) 2 1992 435 443 10.1093/cercor/2.6.435-a 1477524
70. Wittchen H.U., Wunderlich U., Gruschwitz S., Zaudig M. SKID-I. Strukturiertes Klinisches Interview für DSM-IV. Achse I: Psychische Störungen 1997 Hogrefe Göttingen, Germany
71. Yaxley S., Rolls E.T., Sienkiewicz Z.J. The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger Physiology & Behavior 42 1988 223 229 10.1016/0031-9384(88)90074-1 3406148 (Pubitemid 18083964)
72. Zang Z.X., Yan C.G., Dong Z.Y., Huang J., Zang Y.F. Granger causality analysis implementation on MATLAB: a graphic user interface toolkit for fMRI data processing Journal of Neuroscience Methods 203 2012 418 426 22020117
73. Zastrow A., Kaiser S., Stippich C., Walther S., Herzog W., Tchanturia K., Belger A., Weisbrod M., Treasure J., Friederich H.C. Neural correlates of impaired cognitive-behavioral flexibility in anorexia nervosa American Journal of Psychiatry 166 2009 608 616 10.1176/appi.ajp.2008.08050775 19223435
74. Zhou Z., Ding M., Chen Y., Wright P., Lu Z., Liu Y. Detecting directional influence in fMRI connectivity analysis using PCA based Granger causality Brain Research 1289 2009 22 29 10.1016/j.brainres.2009.06.096 19595679
75. Zhou Z., Wang X., Klahr N.J., Liu W., Arias D., Liu H., von Deneen K.M., Wen Y., Lu Z., Xu D., Liu Y. A conditional Granger causality model approach for group analysis in functional magnetic resonance imaging Magnetic Resonance Imaging 29 2011 418 433 10.1016/j.mri.2010.10.008 21232892
76. Zipfel S., Lowe B., Reas D.L., Deter H.C., Herzog W. Long-term prognosis in anorexia nervosa: lessons from a 21-year follow-up study Lancet 355 2000 721 722 10.1016/S0140-6736(99)05363-5 10703806 (Pubitemid 30107630)
77. Zipfel S., Mack I., Baur L.A., Hebebrand J., Touyz S., Herzog W., Abraham S., Davies P.S.W., Russell J. Impact of exercise on energy metabolism in anorexia nervosa Journal of Eating Disorders 1 2013 37 10.1186/2050-2974-1-37 24499685
78. Zipfel S., Wild B., Gross G., Friederich H.C., Teufel M., Schellberg D., Giel K.E., de Zwaan M., Dinkel A., Herpertz S., Burgmer M., Lowe B., Tagay S., von Wietersheim J., Zeeck A., Schade-Brittinger C., Schauenburg H., Herzog W. Focal Psychodynamic Therapy, Cognitive Behaviour Therapy, and Optimised Treatment as Usual in Outpatients with Anorexia Nervosa (ANTOP Study): Randomised Controlled Trial 2013 Lancet
79. Zuo X.N., Ehmke R., Mennes M., Imperati D., Castellanos F.X., Sporns O., Milham M.P. Network centrality in the human functional connectome Cerebral Cortex (New York, N.Y.: 1991) 22 2012 1862 1875 21968567