Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-14T17:23:42.022Z Has data issue: false hasContentIssue false
  • English
  • Français

Brain connectome modularity in weight-restored anorexia nervosa and body dysmorphic disorder

Published online by Cambridge University Press:  19 July 2016

A. Zhang ,
A. Leow ,
L. Zhan ,
J. GadElkarim ,
T. Moody ,
S. Khalsa ,
M. Strober  and
J. D. Feusner
A. Zhang
Affiliation:
Department of Psychiatry, University of Illinois-Chicago, Chicago, IL, USA
A. Leow*
Affiliation:
Department of Psychiatry, University of Illinois-Chicago, Chicago, IL, USA Department of Bioengineering, University of Illinois-Chicago, Chicago, IL, USA The Collaborative Neuroimaging Environment for Connectomics (CoNECt), University of Illinois-Chicago, Chicago, IL, USA
L. Zhan
Affiliation:
Computer Engineering Program, University of Wisconsin-Stout, Menomonie, WI, USA
J. GadElkarim
Affiliation:
Department of Psychiatry, University of Illinois-Chicago, Chicago, IL, USA
T. Moody
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA
S. Khalsa
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA
M. Strober
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA
J. D. Feusner
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, CA, USA
*
*Address for correspondence: A. Leow, M.D., Ph.D., Department of Psychiatry and Bioengineering, University of Illinois College of Medicine, Room 584, 1601 West Taylor Street, Chicago, IL 60612, USA. (Email: [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Anorexia nervosa (AN) and body dysmorphic disorder (BDD) frequently co-occur, and have several overlapping phenomenological features. Little is known about their shared neurobiology. The aim of the study was to compare modular organization of brain structural connectivity.

Method

We acquired diffusion-weighted magnetic resonance imaging data on unmedicated individuals with BDD (n = 29), weight-restored AN (n = 24) and healthy controls (HC) (n = 31). We constructed connectivity matrices using whole-brain white matter tractography, and compared modular structures across groups.

Results

AN showed abnormal modularity involving frontal, basal ganglia and posterior cingulate nodes. There was a trend in BDD for similar abnormalities, but no significant differences compared with AN. In AN, poor insight correlated with longer path length in right caudal anterior cingulate and right posterior cingulate.

Conclusions

Abnormal network organization patterns in AN, partially shared with BDD, may have implications for understanding integration between reward and habit/ritual formation, as well as conflict monitoring/error detection.

Keywords

Anorexia nervosabody dysmorphic disorderconnectomediffusion tensor imaginggraph theorywhite matter
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 13 , October 2016 , pp. 2785 - 2797
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agam, Y, Hamalainen, MS, Lee, AK, Dyckman, KA, Friedman, JS, Isom, M, Makris, N, Manoach, DS (2010). Multimodal neuroimaging dissociates hemodynamic and electrophysiological correlates of error processing. Proceedings of the National Academy of Sciences of the United States of America 108, 17556–17561.CrossRefGoogle Scholar
Alexander-Bloch, AF, Gogtay, N, Meunier, D, Birn, R, Clasen, L, Lalonde, F, Lenroot, R, Giedd, J, Bullmore, ET (2010). Disrupted modularity and local connectivity of brain functional networks in childhood-onset schizophrenia. Frontiers in Systems Neuroscience 4, 147.CrossRefGoogle ScholarPubMed
Altman, SE, Shankman, SA (2009). What is the association between obsessive compulsive disorder and eating disorders? Clinical Psychology Review 29, 638–646.CrossRefGoogle ScholarPubMed
American Psychiatric Association (2000). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR , 4th edn. American Psychiatric Association: Washington, DC.Google Scholar
American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders: DSM-5 , 5th edn. American Psychiatric Publishing: Washington, DC.Google Scholar
Aron, AR (2011). From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry 69, e55–e68.CrossRefGoogle ScholarPubMed
Balleine, BW, Delgado, MR, Hikosaka, O (2007). The role of the dorsal striatum in reward and decision-making. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 27, 8161–8165.CrossRefGoogle ScholarPubMed
Belloch, A, Roncero, M, Perpina, C (2012). Ego-syntonicity and ego-dystonicity associated with upsetting intrusive cognitions. Journal of Psychopathology and Behavioral Assessment 34, 94–106.CrossRefGoogle Scholar
Buhlmann, U, Glaesmer, H, Mewes, R, Fama, JM, Wilhelm, S, Brahler, E, Rief, W (2010). Updates on the prevalence of body dysmorphic disorder: a population-based survey. Psychiatry Research 178, 171–175.CrossRefGoogle ScholarPubMed
Bullmore, E, Sporns, O (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience 10, 186–198.CrossRefGoogle ScholarPubMed
Bullmore, ET, Bassett, DS (2011). Brain graphs: graphical models of the human brain connectome. Annual Review of Clinical Psychology 7, 113–140.Google Scholar
Cooper, MJ, Todd, G, Woolrich, R, Somerville, K, Wells, A (2006). Assessing eating disorder thoughts and behaviors: the development and preliminary evaluation of two questionnaires. Cognitive Therapy and Research 30, 551–570.CrossRefGoogle Scholar
Cororve, MB, Gleaves, DH (2001). Body dysmorphic disorder: a review of conceptualizations, assessment, and treatment strategies. Clinical Psychology Review 21, 949–970.CrossRefGoogle ScholarPubMed
Cowdrey, FA, Park, RJ, Harmer, CJ, McCabe, C (2011). Increased neural processing of rewarding and aversive food stimuli in recovered anorexia nervosa. Biological Psychiatry 70, 736–743.CrossRefGoogle ScholarPubMed
Das, TK, Abeyasinghe, PM, Crone, JS, Sosnowski, A, Laureys, S, Owen, AM, Soddu, A (2014). Highlighting the structure–function relationship of the brain with the Ising model and graph theory. BioMed Research International 2014, 237898.Google ScholarPubMed
Eisen, JL, Phillips, KA, Baer, L, Beer, DA, Atala, KD, Rasmussen, SA (1998). The Brown Assessment of Beliefs Scale: reliability and validity. American Journal of Psychiatry 155, 102–108.CrossRefGoogle ScholarPubMed
Eisen, JL, Phillips, KA, Coles, ME, Rasmussen, SA (2004). Insight in obsessive compulsive disorder and body dysmorphic disorder. Comprehensive Psychiatry 45, 10–15.CrossRefGoogle ScholarPubMed
Fairburn, CG, Cooper, Z, O'Connor M (2008). Eating Disorder Examination (16.0D). In Cognitive Behavior Therapy and Eating Disorders (ed. Fairburn, C. G.). The Guilford Press: New York.Google ScholarPubMed
Frank, GK, Reynolds, JR, Shott, ME, Jappe, L, Yang, TT, Tregellas, JR, O'Reilly, RC (2012). Anorexia nervosa and obesity are associated with opposite brain reward response. Neuropsychopharmacology 37, 2031–2046.CrossRefGoogle ScholarPubMed
Gadelkarim, JJ, Ajilore, O, Schonfeld, D, Zhan, L, Thompson, PM, Feusner, JD, Kumar, A, Altshuler, LL, Leow, AD (2014). Investigating brain community structure abnormalities in bipolar disorder using path length associated community estimation. Human Brain Mapping 35, 2253–2264.CrossRefGoogle ScholarPubMed
Garcia-Soriano, G, Roncero, M, Perpina, C, Belloch, A (2014). Intrusive thoughts in obsessive–compulsive disorder and eating disorder patients: a differential analysis. European Eating Disorders Review 22, 191–199.CrossRefGoogle ScholarPubMed
Grant, JE, Kim, SW, Eckert, ED (2002). Body dysmorphic disorder in patients with anorexia nervosa: prevalence, clinical features, and delusionality of body image. International Journal of Eating Disorders 32, 291–300.CrossRefGoogle ScholarPubMed
Haber, SN, Knutson, B (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4–26.CrossRefGoogle ScholarPubMed
Hamilton, M (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology 32, 50–55.CrossRefGoogle ScholarPubMed
Hartmann, AS, Thomas, JJ, Wilson, AC, Wilhelm, S (2013). Insight impairment in body image disorders: delusionality and overvalued ideas in anorexia nervosa versus body dysmorphic disorder. Psychiatry Research 210, 1129–1135.CrossRefGoogle ScholarPubMed
Kollei, I, Brunhoeber, S, Rauh, E, de Zwaan, M, Martin, A (2012). Body image, emotions and thought control strategies in body dysmorphic disorder compared to eating disorders and healthy controls. Journal of Psychosomatic Research 72, 321–327.CrossRefGoogle ScholarPubMed
Koran, LM, Abujaoude, E, Large, MD, Serpe, RT (2008). The prevalence of body dysmorphic disorder in the United States adult population. CNS Spectrums 13, 316–322.CrossRefGoogle ScholarPubMed
Leow, A, Ajilore, O, Zhan, L, Arienzo, D, GadElkarim, J, Zhang, A, Moody, T, Van Horn, J, Feusner, J, Kumar, A, Thompson, P, Altshuler, L (2012). Impaired inter-hemispheric integration in bipolar disorder revealed with brain network analyses. Biological Psychiatry 73, 183–193.CrossRefGoogle ScholarPubMed
Li, W, Lai, TM, Bohon, C, Loo, SK, McCurdy, D, Strober, M, Bookheimer, S, Feusner, J (2015 a). Anorexia nervosa and body dysmorphic disorder are associated with abnormalities in processing visual information. Psychological Medicine 45, 2111–2122.CrossRefGoogle ScholarPubMed
Li, W, Lai, TM, Loo, SK, Strober, M, Mohammad-Rezazadeh, I, Khalsa, S, Feusner, J (2015 b). Aberrant early visual neural activity and brain–behavior relationships in anorexia nervosa and body dysmorphic disorder. Frontiers in Human Neuroscience 9, 301.CrossRefGoogle ScholarPubMed
Liu, Y, Liang, M, Zhou, Y, He, Y, Hao, Y, Song, M, Yu, C, Liu, H, Liu, Z, Jiang, T (2008). Disrupted small-world networks in schizophrenia. Brain: a Journal of Neurology 131, 945–961.CrossRefGoogle ScholarPubMed
Lynall, ME, Bassett, DS, Kerwin, R, McKenna, PJ, Kitzbichler, M, Muller, U, Bullmore, E (2010). Functional connectivity and brain networks in schizophrenia. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 30, 9477–9487.CrossRefGoogle ScholarPubMed
Mancuso, SG, Knoesen, NP, Castle, DJ (2010). Delusional versus nondelusional body dysmorphic disorder. Comprehensive Psychiatry 51, 177–182.CrossRefGoogle ScholarPubMed
Menzies, L, Chamberlain, SR, Laird, AR, Thelen, SM, Sahakian, BJ, Bullmore, ET (2008). Integrating evidence from neuroimaging and neuropsychological studies of obsessive–compulsive disorder: the orbitofronto-striatal model revisited. Neuroscience and Biobehavioral Reviews 32, 525–549.CrossRefGoogle ScholarPubMed
Montgomery, SA, Åsberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382–389.CrossRefGoogle ScholarPubMed
Moody, TD, Sasaki, MA, Bohon, C, Strober, MA, Bookheimer, SY, Sheen, CL, Feusner, JD (2015). Functional connectivity for face processing in individuals with body dysmorphic disorder and anorexia nervosa. Psychological Medicine 45, 3491–3503.CrossRefGoogle ScholarPubMed
Nambu, A, Tokuno, H, Takada, M (2002). Functional significance of the cortico-subthalamo-pallidal “hyperdirect” pathway. Neuroscience Research 43, 111–117.CrossRefGoogle ScholarPubMed
Newman, ME, Girvan, M (2004). Finding and evaluating community structure in networks. Physical Review E 69, 026113.CrossRefGoogle ScholarPubMed
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113.CrossRefGoogle ScholarPubMed
Peng, ZW, Shi, F, Shi, CZ, Yang, Q, Chan, RCK, Shen, DG (2014). Disrupted cortical network as a vulnerability marker for obsessive–compulsive disorder. Brain Structure and Function 219, 1801–1812.CrossRefGoogle ScholarPubMed
Perpina, C, Roncero, M, Belloch, A, Sanchez-Reales, S (2011). Eating-related intrusive thoughts inventory: exploring the dimensionality of eating disorder symptoms. Psychological Reports 109, 108–126.CrossRefGoogle ScholarPubMed
Phillipou, A, Rossell, SL, Castle, DJ (2014). The neurobiology of anorexia nervosa: a systematic review. Australian and New Zealand Journal of Psychiatry 48, 128–152.CrossRefGoogle ScholarPubMed
Phillips, KA, Atala, KD, Pope, HG Jr. (1995). Diagnostic instruments for body dysmorphic disorder. New research program and abstracts, American Psychiatric Association 148th Annual Meeting; Miami, p. 157.Google Scholar
Phillips, KA, Hollander, E, Rasmussen, SA, Aronowitz, BR, DeCaria, C, Goodman, WK (1997). A severity rating scale for body dysmorphic disorder: development, reliability, and validity of a modified version of the Yale–Brown Obsessive–Compulsive Scale. Psychopharmacology Bulletin 33, 17–22.Google ScholarPubMed
Phillips, KA, Kaye, WH (2007). The relationship of body dysmorphic disorder and eating disorders to obsessive–compulsive disorder. CNS Spectrums 12, 347–358.CrossRefGoogle ScholarPubMed
Rabe-Jablonska, JJ, Sobow T, M (2000). The links between body dysmorphic disorder and eating disorders. European Psychiatry 15, 302–305.CrossRefGoogle Scholar
Rief, W, Buhlmann, U, Wilhelm, S, Borkenhagen, A, Brahler, E (2006). The prevalence of body dysmorphic disorder: a population-based survey. Psychological Medicine 36, 877–885.CrossRefGoogle ScholarPubMed
Ruffolo, J, Phillips, K, Menard, W, Fay, C, Weisberg, R (2006). Comorbidity of body dysmorphic disorder and eating disorders: severity of psychopathology and body image disturbance. International Journal of Eating Disorders 39, 11–19.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59 (Suppl. 20), 22–33; quiz 34–57.Google ScholarPubMed
Sporns, O (2010). Networks of the Brain. MIT Press: Cambridge, MA.CrossRefGoogle Scholar
Steinglass, JE, Eisen, JL, Attia, E, Mayer, L, Walsh, BT (2007). Is anorexia nervosa a delusional disorder? An assessment of eating beliefs in anorexia nervosa. Journal of Psychiatric Practice 13, 65–71.CrossRefGoogle ScholarPubMed
Swinbourne, JM, Touyz, SW (2007). The co-morbidity of eating disorders and anxiety disorders: a review. European Eating Disorders Review 15, 253–274.CrossRefGoogle ScholarPubMed
van den Heuvel, MP, Mandl, RC, Stam, CJ, Kahn, RS, Hulshoff Pol, H (2010). Aberrant frontal and temporal complex network structure in schizophrenia: a graph theoretical analysis. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 30, 15915–15926.CrossRefGoogle ScholarPubMed
Vogt, B (2009). Regions and subregions of the cingulate gyrus. In Cingulate Neurobiology and Disease (ed. Vogt, B.), pp. 3–30. Oxford University Press: Oxford.CrossRefGoogle Scholar
Supplementary material: File

Zhang supplementary material

Zhang supplementary material 1

Download Zhang supplementary material(File)
File 74.1 KB