Abnormal white matter connections between medial frontal regions predict symptoms in patients with first episode schizophrenia

Cortex

Volumn 71, Issue , 2015, Pages 264-276

  Ohtani, Toshiyuki ^a,b,f   Bouix, Sylvain ^a   Lyall, Amanda E ^a   Hosokawa, Taiga ^a,b,g   Saito, Yukiko ^a,h   Melonakos, Eric ^a   Westin, Carl Fredrik ^a   Seidman, Larry J ^c,d   Goldstein, Jill ^d   Mesholam Gately, Raquelle ^c   Petryshen, Tracey ^d,e   Wojcik, Joanne ^d   Kubicki, Marek ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b VA BOSTON HEALTHCARE SYSTEM   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f CHIBA UNIVERSITY   (Japan)

^g Tsuchida Hospital   (Japan)

^h KANSAI MEDICAL UNIVERSITY   (Japan)

Author keywords

Anterior cingulate cortex; First episode schizophrenia; Fractional anisotropy; Orbitofrontal cortex; White matter

Indexed keywords

ATYPICAL ANTIPSYCHOTIC AGENT; NEUROLEPTIC AGENT;

ADOLESCENT; ADULT; ANHEDONIA; ANTERIOR CINGULATE; ARTICLE; CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DELUSION; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; GRAY MATTER; HALLUCINATION; HUMAN; MALE; MEDIAL ORBITOFRONTAL CORTEX; NEUROLOGIC DISEASE ASSESSMENT; SCALE FOR THE ASSESSMENT OF NEGATIVE SYMPTOM; SCALE FOR THE ASSESSMENT OF POSITIVE SYMPTOM; SCHIZOPHRENIA; STOCHASTIC TRACTOGRAPHY; TRACTOGRAPHY; WHITE MATTER; WHITE MATTER ABNORMALITY; AFFECT; ANISOTROPY; CINGULATE GYRUS; DELUSIONS; FRONTAL LOBE; HALLUCINATIONS; ONSET AGE; PATHOLOGY; PREDICTIVE VALUE; PSYCHOLOGICAL RATING SCALE; PSYCHOLOGY; SOCIAL BEHAVIOR; YOUNG ADULT;

ADOLESCENT; ADULT; AFFECT; AGE OF ONSET; ANHEDONIA; ANISOTROPY; ANTIPSYCHOTIC AGENTS; DELUSIONS; DIFFUSION TENSOR IMAGING; FEMALE; FRONTAL LOBE; GRAY MATTER; GYRUS CINGULI; HALLUCINATIONS; HUMANS; MALE; PREDICTIVE VALUE OF TESTS; PSYCHIATRIC STATUS RATING SCALES; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; SOCIAL BEHAVIOR; WHITE MATTER; YOUNG ADULT;

EID: 84940173186     PISSN: 00109452     EISSN: 19738102     Source Type: Journal    
DOI: 10.1016/j.cortex.2015.05.028     Document Type: Article

References (83)

1. Alexander A.L., Tsuruda J.S., Parker D.L. Elimination of eddy current artifacts in diffusion-weighted echo-planar images: the use of bipolar gradients. Magnetic Resonance in Medicine 1997, 38:1016-1021.
2. Allen P., Amaro E., Fu C.H., Williams S.C., Brammer M.J., Johns L.C., et al. Neural correlates of the misattribution of speech in schizophrenia. British Journal of Psychiatry 2007, 190:162-169.
3. Allman J.M., Hakeem A., Erwin J.M., Nimchinsky E., Hof P. The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Annals of the New York Academy of Sciences 2001, 935:107-117.
4. Andreasen N.C. Scale for the assessment of negative symptoms (SANS) 1981, University of Iowa College of Medicine, Iowa (IA).
5. Andreasen N.C. Scale for the assessment of positive symptoms (SAPS) 1984, Department of Psychiatry, University of Iowa College of medicine, Iowa City, IA.
6. Baron-Cohen S., Ring H., Moriarty J., Schmitz B., Costa D., Ell P. Recognition of mental state terms. Clinical findings in children with autism and a functional neuroimaging study of normal adults. British Journal of Psychiatry 1994, 165:640-649.
7. Berlin H.A., Rolls E.T., Kischka U. Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. Brain 2004, 127(Pt 5):1108-1126.
8. Björnemo M., Brun A., Kikinis R., Westin C.F. Regularized stochastic white matter tractography using diffusion tensor MRI. Fifth Int Conf on Med Image Computing and Computer-Assisted Intervention (MICCAI'02) 2002, 435-442.
9. Blackwood N.J., Bentall R.P., Ffytche D.H., Simmons A., Murray R.M., Howard R.J. Persecutory delusions and the determination of self-relevance: an fMRI investigation. Psychologie Medicale 2004, 34:591-596.
10. Brüne M., Lissek S., Fuchs N., Witthaus H., Peters S., Nicolas V., et al. An fMRI study of theory of mind in schizophrenic patients with "passivity" symptoms. Neuropsychologia 2008, 46(7):1992-2001.
11. Brunet E., Sarfati Y., Hardy-Baylé M.C., Decety J. A PET investigation of the attribution of intentions with a nonverbal task. NeuroImage 2000, 11(2):157-166.
12. Buchy L., Ad-Dab'bagh Y., Lepage C., Malla A., Joober R., Evans A., et al. Symptom attribution in first episode psychosis: a cortical thickness study. Psychiatry Research 2012, 203(1):6-13.
13. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 2000, 4(6):215-222.
14. Caligiuri M.P., Hellige J.B., Cherry B.J., Kwok W., Lulow L.L., Lohr J.B. Lateralized cognitive dysfunction and psychotic symptoms in schizophrenia. Schizophrenia Research 2005, 80(2-3):151-161.
15. Cheung V., Cheung C., McAlonan G.M., Deng Y., Wong J.G., Yip L., et al. A diffusion tensor imaging study of structural dysconnectivity in never-medicated, first-episode schizophrenia. Psychological Medicine 2008, 38:877-885.
16. Cleghorn J.M., Franco S., Szechtman B., Kaplan R.D., Szechtman H., Brown G.M., et al. Toward a brain map of auditory hallucinations. American Journal of Psychiatry 1992, 149(8):1062-1069.
17. Critchley H.D. Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology 2005, 493:154-166.
18. Critchley H.D., WIens S., Rotshtein P., Ohman A., Dolan R.J. Neural systems supporting interoceptive awareness. Nature Neuroscience 2004, 7:189-195.
19. Cui L., Chen Z., Deng W., Huang X., Li M., Ma X., et al. Assessment of white matter abnormalities in paranoid schizophrenia and bipolar mania patients. Psychiatry Research 2011, 194(3):347-353.
20. Davis K.L., Stewart D.G., Friedman J.I., Buchsbaum M., Harvey P.D., Hof P.R., et al. White matter changes in schizophrenia: evidence for myelin-related dysfunction. Archives of General Psychiatry 2003, 60:443-456.
21. Dekker N., Schmitz N., Peters B.D., van Amelsvoort T.A., Linszen D.H., de Haan L. Cannabis use and callosal white matter structure and integrity in recent-onset schizophrenia. Psychiatry Research 2010, 181(1):51-56.
22. Duda J.T., McMillan C., Grossman M., Gee J.C. Relating structural and functional connectivity to performance in a communication task. Medical Image Computing and Computer-Assisted Intervention 2010, 13(Pt 2):282-289.
23. Diekhof E.K., Falkai P., Gruber O. The orbitofrontal cortex and its role in the assignment of behavioural significance. Neuropsychologia 2011, 49(5):984-991.
24. Elliott R., Rubinsztein J.S., Sahakian B.J., Dolan R.J. The neural basis of mood-congruent processing biases in depression. Archives of General Psychiatry 2002, 59(7):597-604.
25. Erkwoh R., Sabri O., Steinmeyer E.M., Bull U., Sass H. Psychopathological and SPECT findings in never-treated schizophrenia. Acta Psychiatrica Scandinavica 1997, 96:51-57.
26. Federspiel A., Begré S., Kiefer C., Schroth G., Strik W.K., Dierks T. Alterations of white matter connectivity in first episode schizophrenia. Neurobiology of Disease 2006, 22:702-709.
27. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P) 2002, Biometrics Research, New York State Psychiatric Institute, New York.
28. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition (SCID-I/NP) 2002, Biometrics Research, New York State Psychiatric Institute, New York.
29. Fitzsimmons J., Hamoda H.M., Swisher T., Terry D., Rosenberger G., Seidman L.J., et al. Diffusion tensor imaging study of the fornix in first episode schizophrenia and in healthy controls. Schizophrenia Research 2014, 156(2-3):157-160.
30. Foucher J.R., Vidailhet P., Chanraud S., Gounot D., Grucker D., Pins D., et al. Functional integration in schizophrenia: too little or too much? Preliminary results on fMRI data. NeuroImage 2005, 26(2):374-388.
31. Gasparotti R., Valsecchi P., Carletti F., Galluzzo A., Liserre R., Cesana B., et al. Reduced fractional anisotropy of corpus callosum in first-contact, antipsychotic drug-naive patients with schizophrenia. Schizophrenia Research 2009, 108(1-3):41-48.
32. Gladsjo J.A., Heaton R.K., Palmer B.W., Taylor M.J., Jeste D.V. Use of oral reading to estimate premorbid intellectual and neuropsychological functioning. Journal of the International Neuropsychological Society 1999, 5(3):247-254.
33. Goldstein R.Z., Tomasi D., Rajaram S., Cottone L.A., Zhang L., Maloney T., et al. Role of the anterior cingulate and medial orbitofrontal cortex in processing drug cues in cocaine addiction. Neuroscience 2007, 144:1153-1159.
34. Hao Y., Liu Z., Jiang T., Gong G., Liu H., Tan L., et al. White matter integrity of the whole brain is disrupted in first-episode schizophrenia. NeuroReport 2006, 17:23-26.
35. Heid O. Eddy current-nulled diffusion weighting. Proc Int Soc Mag Reson Med, Denver, CO, p. 799. Med 2000, 38:1016-1021.
36. Hien D., Matzner F.J., First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured clinical interview for DSM-IV-Child edition (Version 1.0) 1994, Columbia University, New York.
37. Hubl D., Koenig T., Strik W., Federspiel A., Kreis R., Boesch C., et al. Pathways that make voices: white matter changes in auditory hallucinations. Archives of General Psychiatry 2004, 61(7):658-668.
38. Hughes B.L., Beer J.S. Orbitofrontal cortex and anterior cingulate cortex are modulated by motivated social cognition. Cerebral Cortex 2012, 22(6):1372-1381.
39. Kanaan R., Barker G., Brammer M., Giampietro V., Shergill S., Woolley J., et al. White matter microstructure in schizophrenia: effects of disorder, duration and medication. British Journal of Psychiatry 2009, 194(3):236-242.
40. Kapur S. Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry 2003, 160(1):12-23.
41. Karlsgodt K.H., van Erp T.G., Poldrack R.A., Bearden C.E., Nuechterlein K.H., Cannon T.D. Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biological Psychiatry 2008, 63:512-518.
42. Kawashima T., Nakamura M., Bouix S., Kubicki M., Salisbury D.F., Westin C.F., et al. Uncinate fasciculus abnormalities in recent onset schizophrenia and affective psychosis: a diffusion tensor imaging study. Schizophrenia Research 2009, 2009(110):119-126.
43. Konrad A., Winterer G. Disturbed structural connectivity in schizophrenia primary factor in pathology or epiphenomenon?. Schizophrenia Bulletin 2008, 34(1):72-92.
44. Kreher B.W., Schnell S., Mader I., Il'yasov K.A., Hennig J., Kiselev V.G., et al. Connecting and merging fibres: pathway extraction by combining probability maps. NeuroImage 2008, 43:81-89.
45. Kubicki M., Alvarado J.L., Westin C.F., Tate D.F., Markant D., Terry D.P., et al. Stochastic tractography study of inferior frontal gyrus anatomical connectivity in schizophrenia. NeuroImage 2011, 55:1657-1664.
46. Kubicki M., McCarley R., Westin C.F., Park H.J., Maier S., Kikinis R., et al. A review of diffusion tensor imaging studies in schizophrenia. Journal of Psychiatric Research 2007, 41:15-30.
47. Lahti A.C., Weiler M.A., Holcomb H.H., Tamminga C.A., Carpenter W.T., McMahon R. Correlations between rCBF and symptoms in two independent cohorts of drug-free patients with schizophrenia. Neuropsychopharmacology 2006, 31:221-230.
48. Liu J.X.., Chen Y.S., Hsieh J.C., Su T.P., Yeh T.C., Chen L.F. Differences in white matter abnormalities between bipolar I and II disorders. Journal of Affective Disorders 2010, 127(1-3):309-315.
49. Liu X., Lai Y., Wang X., Hao C., Chen L., Zhou Z., et al. Reduced white matter integrity and cognitive deficit in never-medicated chronic schizophrenia: a diffusion tensor study using TBSS. Behavioural Brain Research 2013, 252:157-163.
50. de Marco G., de Bonis M., Vrignaud P., Henry-Feugeas M.C., Peretti I. Changes in effective connectivity during incidental and intentional perception of fearful faces. NeuroImage 2006, 30(3):1030-1037.
51. Mitelman S.A., Torosjan Y., Newmark R.E., Schneiderman J.S., Chu K.W., Brickman A.M., et al. Internal capsule, corpus callosum and long associative fibers in good and poor outcome schizophrenia: a diffusion tensor imaging survey. Schizophrenia Research 2007, 92(1-3):211-224.
52. Mori S., Wakana S., van Zijl P.C.M., Nagae-Poetscher L.M. MRI atlas of human white matter 2005, Elsevier Inc, CA, USA.
53. Ohtani T., Bouix S., Hosokawa T., Saito Y., Eckbo R., Ballinger T., et al. Abnormalities in white matter connections between orbitofrontal cortex and anterior cingulate cortex and their associations with negative symptoms in schizophrenia: a DTI study. Schizophrenia Research 2014, 157(1-3):190-197.
54. Oishi K., Konishi J., Mori S., Ishihara H., Kawamitsu H., Fujii M., et al. Reduced fractional anisotropy in early-stage cerebellar variant of multiple system atrophy. Journal of Neuroimaging 2009, 19(2):127-131.
55. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
56. Palaniyappan L., Mallikarjun P., Joseph V., White T.P., Liddle P.F. Reality distortion is related to the structure of the salience network in schizophrenia. Psychological Medicine 2011, 41(8):1701-1708.
57. Parellada E., Lomena F., Font M., Pareto D., Gutierrez F., Simo M., et al. Fluordeoxyglucose-PET study in first-episode schizophrenic patients during the hallucinatory state, after remission and during linguistic-auditory activation. Nuclear Medicine Communications 2008, 29(10):894-900.
58. Pérez-Iglesias R., Tordesillas-Gutiérrez D., McGuire P.K., Barker G.J., Roiz-Santiañez R., Mata I., et al. White matter integrity and cognitive impairment in first-episode psychosis. American Journal of Psychiatry 2010, 167(4):451-458.
59. Peters B.D., Blaas J., de Haan L. Diffusion tensor imaging in the early phase of schizophrenia: what have we learned?. Journal of Psychiatric Research 2010, 44(15):993-1004.
60. Peters B.D., de Haan L., Dekker N., Blaas J., Becker H.E., Dingemans P.M., et al. White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology 2008, 58(1):19-28.
61. Pettersson-Yeo W., Allen P., Benetti S., McGuire P., Mechelli A. Dysconnectivity in schizophrenia: where are we now?. Neuroscience & Biobehavioral Reviews 2011, 35(5):1110-1124.
62. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage 2002, 16(2):331-348.
63. Price G., Cercignani M., Parker G.J., Altmann D.R., Barnes T.R., Barker G.J., et al. Abnormal brain connectivity in first-episode psychosis: a diffusion MRI tractography study of the corpus callosum. NeuroImage 2007, 35:458-466.
64. Rotarska-Jagiela A., Schönmeyer R., Oertel V., Haenschel C., Vogeley K., Linden D.E. The corpus callosum in schizophrenia-volume and connectivity changes affect specific regions. NeuroImage 2008, 39(4):1522-1532.
65. Roy K., Murtie J.C., El-Khodor B.F., Edgar N., Sardi S.P., Hooks B.M., et al. Loss of erbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(19):8131-8136.
66. Rudebeck P.H., Bannerman D.M., Rushworth M.F. The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making. Cognitive, Affective, & Behavioral Neuroscience 2008, 8(4):485-497.
67. Rudebeck P.H., Behrens T.E., Kennerley S.W., Baxter M.G., Buckley M.J., Walton M.E., et al. Frontal cortex subregions play distinct roles in choices between actions and stimuli. Journal of Neuroscience 2008, 28(51):13775-13785.
68. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., et al. Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience 2007, 27(9):2349-2356.
69. Segal D., Koschnick J.R., Slegers L.H., Hof P.R. Oligodendrocyte pathophysiol-ogy: a new view of schizophrenia. International Journal of Neuropsychopharmacology 2007, 10:503-511.
70. Seok J.H., Park H.J., Chun J.W., Lee S.K., Cho H.S., Kwon J.S., et al. White matter abnormalities associated with auditory hallucinations in schizophrenia: a combined study of voxel-based analyses of diffusion tensor imaging and structural magnetic resonance imaging. Psychiatry Research 2007, 156(2):93-104.
71. Shad M.U., Muddasani S., Keshavan M.S. Prefrontal subregions and dimensions of insight in first-episode schizophrenia-a pilot study. Psychiatry Research 2006, 146(1):35-42.
72. Silbersweig D.A., Stern E., Frith C., Cahill C., Holmes A., Grootoonk S., et al. A functional neuroanatomy of hallucinations in schizophrenia. Nature 1995, 378(6553):176-179.
73. Song S.K., Sun S.W., Ju W.K., Lin S.J., Cross A.H., Neufeld A.H. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. NeuroImage 2003, 20(3):1714-1722.
74. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 2002, 17(3):1429-1436.
75. Szeszko P.R., Robinson D.G., Ashtari M., Vogel J., Betensky J., Sevy S., et al. Clinical and neuropsychological correlates of white matter abnormalities in recent onset schizophrenia. Neuropsychopharmacology 2008, 33(5):976-984.
76. Tang J., Liao Y., Zhou B., Tan C., Liu T., Hao W., et al. Abnormal anterior cingulum integrity in first episode, early-onset schizophrenia: a diffusion tensor imaging study. Brain Research 2010, 1343:199-205.
77. Uranova N.A., Vostrikov V.M., Vikhreva O.V., Zimina I.S., Kolomeets N.S., Orlovskaya D.D. The role of oligodendrocyte pathology in schizophrenia. International Journal of Neuropsychopharmacology 2007, 10(4):537-545.
78. Völlm B.A., Taylor A.N., Richardson P., Corcoran R., Stirling J., McKie S., et al. Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage 2006, 29(1):90-98.
79. Walter H., Adenzato M., Ciaramidaro A., Enrici I., Pia L., Bara B.G. Understanding intentions in social interaction: the role of the anterior paracingulate cortex. Journal of Cognitive Neuroscience 2004, 16(10):1854-1863.
80. Whitford T.J.., Kubicki M., Ghorashi S., Schneiderman J.S., Hawley K.J., McCarley R.W., et al. Predicting inter-hemispheric transfer time from the diffusion properties of the corpus callosum in healthy individuals and schizophrenia patients: a combined ERP and DTI study. NeuroImage 2011, 54(3):2318-2329.
81. Woods S.W. Chlorpromazine equivalent doses for the newer atypical antipsychotics. Journal of Clinical Psychiatry 2003, 64(6):663-667.
82. Zhang X., Stein E.A., Hong L.E. Smoking and schizophrenia independently and additively reduce white matter integrity between striatum and frontal cortex. Biological Psychiatry 2010, 68(7):674-677.
83. Zou L.Q., Xie J.X., Yuan H.S., Pei X.L., Dong W.T., Liu P.C. Diffusion tensor imaging study of the anterior limb of internal capsules in neuroleptic-naive schizophrenia. Academic Radiology 2008, 15:285-289.