Structural disruption of the dorsal cingulum bundle is associated with impaired Stroop performance in patients with schizophrenia

Previous diffusion tensor imaging (DTI) studies have shown structural abnormalities of the cingulum bundle (CB) in patients with schizophrenia. However, regional specificity and functional relevance of the pregenual and dorsal CB subdivisions has not been fully studied. In the current study, 31 patients with schizophrenia and 65 age- and gender-matched healthy subjects underwent DTI to measure fractional anisotropy (FA) and mean diffusivity (MD) in cross sections of dorsal and pregenual CB tractography. To test the hypothesis of region-specific association with neurocognition, all of the patients and 31 controls performed the Stroop task, which is assumed to mainly involve dorsal cingulate function. The verbal memory subscale of Wechsler Memory Scale-Revised and premorbid IQs estimated from the Japanese version of the National Adult Reading Test, which were non-specific to dorsal cingulate function, were also employed as control neurocognitive indices. Significant bilateral FA reductions in the pregenual and dorsal CB, and bilateral MD increases in the dorsal CB were observed in the patients compared with the controls. As predicted, significant associations between DTI measures and neurocognition were found in the schizophrenia group only: double-dissociable correlation between higher MD in the dorsal, not in the pregenual CB, and a longer reaction time in the Stroop task, not verbal memory or premorbid IQs. The current DTI study suggests that structural disruption of the dorsal CB has region-specific functional relevance to selective attention deficits, although structural disruption also exists in the pregenual CB in patients with schizophrenia.

[1]  Osamu Abe,et al.  Disrupted integrity of the fornix is associated with impaired memory organization in schizophrenia , 2008, Schizophrenia Research.

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

[3]  Jonathan D. Cohen,et al.  Decreased conflict- and error-related activity in the anterior cingulate cortex in subjects with schizophrenia. , 2005, The American journal of psychiatry.

[4]  Colin M. Macleod.  Half a century of research on the Stroop effect: an integrative review. , 1991, Psychological bulletin.

[5]  O. Abe,et al.  MR diffusion tensor imaging: recent advance and new techniques for diffusion tensor visualization. , 2003, European journal of radiology.

[6]  Bruce Fischl,et al.  Reduced microstructural integrity of the white matter underlying anterior cingulate cortex is associated with increased saccadic latency in schizophrenia , 2007, NeuroImage.

[7]  Jonathan D. Cohen,et al.  Interference and Facilitation Effects during Selective Attention: An H2 15O PET Study of Stroop Task Performance , 1995, NeuroImage.

[8]  J. Allardyce,et al.  Nithsdale schizophrenia surveys 21: A longitudinal study of national adult reading test stability , 2000, Schizophrenia Research.

[9]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[10]  S. Skare,et al.  Abnormal brain white matter in schizophrenia: a diffusion tensor imaging study , 2001, Neuroreport.

[11]  Marek Kubicki,et al.  Attentional networks and cingulum bundle in chronic schizophrenia , 2007, Schizophrenia Research.

[12]  Karl J. Friston,et al.  Investigations of the functional anatomy of attention using the stroop test , 1993, Neuropsychologia.

[13]  J. Stroop.  Studies of interference in serial verbal reactions. , 1992 .

[14]  M. First,et al.  Structured clinical interview for DSM-IV axis I disorders : SCID-I : clinical version : scoresheet , 1997 .

[15]  T. Ohnishi,et al.  Progressive changes of white matter integrity in schizophrenia revealed by diffusion tensor imaging , 2007, Psychiatry Research: Neuroimaging.

[16]  M. Raichle,et al.  The anterior cingulate cortex mediates processing selection in the Stroop attentional conflict paradigm. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. Javitt,et al.  BRAIN IMAGING NEUROREPORT , 2005 .

[18]  The White Matter Integrity Disruption in Schizophrenia , 2006 .

[19]  J. Breeze,et al.  Abnormal anterior cingulum in patients with schizophrenia: a diffusion tensor imaging study , 2003, Neuroreport.

[20]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[21]  Dennis Velakoulis,et al.  Anterior cingulate activation during Stroop task performance: a PET to MRI coregistration study of individual patients with schizophrenia. , 2002, The American journal of psychiatry.

[22]  Zhiguo Sun,et al.  Anterior cingulum abnormalities in male patients with schizophrenia determined through diffusion tensor imaging. , 2004, The American journal of psychiatry.

[23]  R. Kikinis,et al.  Cingulate fasciculus integrity disruption in schizophrenia: a magnetic resonance diffusion tensor imaging study , 2003, Biological Psychiatry.

[24]  Osamu Abe,et al.  Human brain structural change related to acute single exposure to sarin , 2007, Annals of neurology.

[25]  S. Lawrie,et al.  Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study , 2003, British Journal of Psychiatry.

[26]  Felix M Mottaghy,et al.  Brain activation patterns during a selective attention test—a functional MRI study in healthy volunteers and patients with schizophrenia , 2003, Psychiatry Research: Neuroimaging.

[27]  M. Bell,et al.  Concurrent validity of the cognitive component of schizophrenia: Relationship of PANSS scores to neuropsychological assessments , 1994, Psychiatry Research.

[28]  Adam M. Brickman,et al.  Internal capsule, corpus callosum and long associative fibers in good and poor outcome schizophrenia: A diffusion tensor imaging survey , 2007, Schizophrenia Research.

[29]  Thomas E. Nichols,et al.  Anterior cingulate gyrus dysfunction and selective attention deficits in schizophrenia: [15O]H2O PET study during single-trial Stroop task performance. , 1997, The American journal of psychiatry.

[30]  G. Barker,et al.  Investigating regional white matter in schizophrenia using diffusion tensor imaging , 2002, Neuroreport.

[31]  Hidenao Fukuyama,et al.  Anterior and posterior cingulum abnormalities and their association with psychopathology in schizophrenia: A diffusion tensor imaging study , 2007, Schizophrenia Research.

[32]  Osamu Abe,et al.  Quantitative evaluation of the pyramidal tract segmented by diffusion tensor tractography: feasibility study in patients with amyotrophic lateral sclerosis. , 2005, Radiation medicine.

[33]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .

[34]  Claude Alain,et al.  Neurophysiological evidence of error-monitoring deficits in patients with schizophrenia. , 2002, Cerebral cortex.

[35]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[36]  M. Sugishita,et al.  Learning Chinese Characters May Improve Visual Recall , 2001, Perceptual and motor skills.

[37]  藤原 広臨,et al.  Anterior cingulate pathology and social cognition in schizophrenia : a study of gray matter, white matter and sulcal morphometry , 2009 .

[38]  K. Kasai,et al.  Estimation of premorbid IQ in individuals with Alzheimer’s disease using Japanese ideographic script (Kanji) compound words: Japanese version of National Adult Reading Test , 2006, Psychiatry and clinical neurosciences.

[39]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[40]  M S Buchsbaum,et al.  MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia , 1998, Neuroreport.

[41]  Tianzi Jiang,et al.  White matter integrity of the whole brain is disrupted in first-episode schizophrenia , 2006, Neuroreport.

[42]  K. Kasai,et al.  The function of selective attention to non-emotional and emotional information in patients with schizophrenia , 2007 .

[43]  S. Rauch,et al.  The counting stroop: An interference task specialized for functional neuroimaging—validation study with functional MRI , 1998, Human brain mapping.