Grey matter abnormalities within cortico-limbic-striatal circuits in acute and weight-restored anorexia nervosa patients

Functional disturbances within cortico-striatal control systems have been implicated in the psychobiology (i.e. impaired cognitive-behavioral flexibility, perfectionist personality) of anorexia nervosa. The aim of the present study was to investigate the morphometry of brain regions within cortico-striatal networks in acute anorexia nervosa (AN) as well as long-term weight-restored anorexia nervosa (AN-WR) patients. A total of 39 participants: 12 AN, 13 AN-WR patients, and 14 healthy controls (HC) underwent high-resolution, T1-weighted magnetic resonance imaging (MRI), a cognitive-behavioral flexibility task, and a psychometric assessment. Group differences in local grey matter volume (GMV) were analyzed using whole brain voxel-based morphometry (VBM) and brain-atlas based automatic volumetry computation (IBASPM). Individual differences in total GMV were considered as a covariate in all analyses. In the regional brain morphometry, AN patients, as compared to HC, showed decreased GMVs (VBM and volumetry) in the anterior cingulate cortex (ACC), the supplementary motor area (SMA), and in subcortical regions (amygdala, putamen: VBM only). AN-WR compared to HC showed decreased GMV (VBM and volumetry) in the ACC and SMA, whereas GMV of the subcortical region showed no differences. The findings of the study suggest that structural abnormalities of the ACC and SMA were independent of the disease stage, whereas subcortical limbic-striatal changes were state dependent.

[1]  Phil J. Greer,et al.  Normal Brain Tissue Volumes after Long-Term Recovery in Anorexia and Bulimia Nervosa , 2006, Biological Psychiatry.

[2]  M. Weisbrod,et al.  Memory performance in acute and weight-restored anorexia nervosa patients , 2010, Psychological Medicine.

[3]  V. Glauche,et al.  Voxel-based morphometry in eating disorders: Correlation of psychopathology with grey matter volume , 2010, Psychiatry Research: Neuroimaging.

[4]  Christian Gaser,et al.  Neuroanatomical correlates of different vulnerability states for psychosis and their clinical outcomes. , 2009, The British journal of psychiatry : the journal of mental science.

[5]  A. Belger,et al.  Neural correlates of impaired cognitive-behavioral flexibility in anorexia nervosa. , 2009, The American journal of psychiatry.

[6]  Maria I. Argyropoulou,et al.  Periventricular leukomalacia in preterm children: assessment of grey and white matter and cerebrospinal fluid changes by MRI , 2009, Pediatric Radiology.

[7]  Vijay K. Venkatraman,et al.  Altered reward processing in women recovered from anorexia nervosa. , 2007, The American journal of psychiatry.

[8]  Timothy E. J. Behrens,et al.  Optimal decision making and the anterior cingulate cortex , 2006, Nature Neuroscience.

[9]  R. Snaith,et al.  The hospital anxiety and depression scale. , 2013, Acta psychiatrica Scandinavica.

[10]  Z. Shahrivar,et al.  Structured Clinical Interview for DSM-IV (SCID): Persian Translation and Cultural Adaptation , 2007 .

[11]  N. Wray,et al.  Shared Temperament Risk Factors for Anorexia Nervosa: A Twin Study , 2008, Psychosomatic medicine.

[12]  Dieter Vaitl,et al.  Regional grey matter volume abnormalities in bulimia nervosa and binge-eating disorder , 2010, NeuroImage.

[13]  Josef Brozek,et al.  The Biology of Human Starvation. , 1950 .

[14]  Julie L. Fudge,et al.  New insights into symptoms and neurocircuit function of anorexia nervosa , 2009, Nature Reviews Neuroscience.

[15]  B. Peterson,et al.  Functional disturbances within frontostriatal circuits across multiple childhood psychopathologies. , 2009, The American journal of psychiatry.

[16]  Blake A. Richards,et al.  Cognitive Function and Brain Structure in Females With a History of Adolescent-Onset Anorexia Nervosa , 2008, Pediatrics.

[17]  K. Krishnan,et al.  Subcortical brain anatomy in anorexia and bulimia , 1992, Biological Psychiatry.

[18]  D. Ståhl,et al.  A systematic review and meta-analysis of set-shifting ability in eating disorders , 2007, Psychological Medicine.

[19]  Christian Gaser,et al.  Gray matter decrease of the anterior cingulate cortex in anorexia nervosa. , 2007, The American journal of psychiatry.

[20]  Steven C. R. Williams,et al.  Recovery and chronicity in anorexia nervosa brain activity associated with differential outcomes , 2003, Biological Psychiatry.

[21]  Carolyn C. Meltzer,et al.  Increased Dopamine D2/D3 Receptor Binding After Recovery from Anorexia Nervosa Measured by Positron Emission Tomography and [11C]Raclopride , 2005, Biological Psychiatry.

[22]  H. Steinhausen.  The outcome of anorexia nervosa in the 20th century. , 2002, The American journal of psychiatry.

[23]  Boris Suchan,et al.  Reduction of gray matter density in the extrastriate body area in women with anorexia nervosa , 2010, Behavioural Brain Research.

[24]  J. Hein,et al.  Are there specific disabilities of number processing in adolescent patients with Anorexia nervosa? Evidence from clinical and neuropsychological data when compared to morphometric measures from magnetic resonance imaging , 2009, European Child & Adolescent Psychiatry.

[25]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[26]  F. Sardanelli,et al.  Volume measurement with magnetic resonance imaging of hippocampus-amygdala formation in patients with anorexia nervosa , 2001, Journal of endocrinological investigation.

[27]  D J Mikulis,et al.  Cerebral gray matter volume deficits after weight recovery from anorexia nervosa. , 1997, Archives of general psychiatry.

[28]  N. Sadowsky,et al.  The prognostic value of initial EDI scores in anorexia nervosa patients: a prospective follow-up study of 5–10 years , 2001, European Psychiatry.

[29]  B. Löwe,et al.  Measuring depression outcome with a brief self-report instrument: sensitivity to change of the Patient Health Questionnaire (PHQ-9). , 2004, Journal of affective disorders.

[30]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[31]  M. Nakajo,et al.  Comparison of regional cerebral blood flow in patients with anorexia nervosa before and after weight gain , 2005, Psychiatry Research: Neuroimaging.

[32]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[33]  J L Rapoport,et al.  The role of the anterior cingulate in automatic and controlled processes: a developmental neuroanatomical study. , 1997, Developmental psychobiology.

[34]  G. Pagnoni,et al.  Human Striatal Response to Salient Nonrewarding Stimuli , 2003, The Journal of Neuroscience.

[35]  Tohru Shiga,et al.  Abnormal neuronal network in anorexia nervosa studied with I-123-IMP SPECT , 2001, Psychiatry Research: Neuroimaging.

[36]  H. Doll,et al.  Risk factors for anorexia nervosa: three integrated case-control comparisons. , 1999, Archives of general psychiatry.

[37]  J. Treasure,et al.  Exploring the neurocognitive signature of poor set-shifting in anorexia and bulimia nervosa. , 2010, Journal of psychiatric research.

[38]  O. Hikosaka,et al.  Perceptual Learning, Motor Learning and Automaticity Switching from Automatic to Controlled Behavior: Cortico-basal Ganglia Mechanisms , 2022 .

[39]  J. Peuskens,et al.  Action monitoring and perfectionism in anorexia nervosa , 2007, Brain and Cognition.

[40]  Julie C Price,et al.  Reduced 5-HT2A receptor binding after recovery from anorexia nervosa , 2002, Biological Psychiatry.

[41]  S. Williams,et al.  Hippocampal volume and cognitive function in anorexia nervosa , 2006, Psychiatry Research: Neuroimaging.

[42]  K. Felmingham,et al.  Mapping frontal-limbic correlates of orienting to change detection , 2007, Neuroreport.

[43]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Nancy Andreasen,et al.  Implications of starvation-induced change in right dorsal anterior cingulate volume in anorexia nervosa. , 2008, The International journal of eating disorders.

[45]  J. Carter,et al.  Perfectionism in anorexia nervosa: a 6-24-month follow-up study. , 2003, The International journal of eating disorders.

[46]  L. Heimer.  A new anatomical framework for neuropsychiatric disorders and drug abuse. , 2003, The American journal of psychiatry.

[47]  J. Castro-Fornieles,et al.  A cross-sectional and follow-up voxel-based morphometric MRI study in adolescent anorexia nervosa. , 2009, Journal of psychiatric research.

[48]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[49]  K. Kiehl,et al.  A supramodal limbic‐paralimbic‐neocortical network supports goal‐directed stimulus processing , 2005, Human brain mapping.

[50]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[51]  S. Rabe-Hesketh,et al.  Childhood obsessive-compulsive personality traits in adult women with eating disorders: defining a broader eating disorder phenotype. , 2003, The American journal of psychiatry.

[52]  R. Kessler,et al.  The Prevalence and Correlates of Eating Disorders in the National Comorbidity Survey Replication , 2007, Biological Psychiatry.

[53]  A. Keys,et al.  The Biology of Human Starvation: Volume I , 1950 .

[54]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[55]  Janet Treasure,et al.  Anorexia nervosa: valued and visible. A cognitive-interpersonal maintenance model and its implications for research and practice. , 2006, The British journal of clinical psychology.

[56]  David F. Tate,et al.  Reliability and validity of MRI-based automated volumetry software relative to auto-assisted manual measurement of subcortical structures in HIV-infected patients from a multisite study , 2010, NeuroImage.

[57]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[58]  D. Collier,et al.  Is impaired set-shifting an endophenotype of anorexia nervosa? , 2005, The American journal of psychiatry.

[59]  J. Cummings,et al.  Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update. , 2002, Journal of psychosomatic research.

[60]  V. Kumari,et al.  Differential motivational responses to food and pleasurable cues in anorexia and bulimia nervosa: a startle reflex paradigm , 2006, Psychological Medicine.

[61]  R. Spitzer,et al.  The PHQ-9: validity of a brief depression severity measure. , 2001, Journal of general internal medicine.

[62]  A. David,et al.  Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies , 2008, Brain Research Reviews.

[63]  O. A. Andreassen,et al.  The human amygdala is involved in general behavioral relevance detection: Evidence from an event-related functional magnetic resonance imaging Go-NoGo task , 2008, Neuroscience.

[64]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[65]  D. Nutzinger,et al.  [A German version of the Eating Disorder Inventory EDI-2]. , 1997, Psychotherapie, Psychosomatik, medizinische Psychologie.