Excessive extracellular volume reveals a neurodegenerative pattern in schizophrenia onset

Journal of Neuroscience

Volumn 32, Issue 48, 2012, Pages 17365-17372

  Pasternak, Ofer ^a   Westin, Carl Fredrik ^a   Bouix, Sylvain ^a   Seidman, Larry J ^b,d   Goldstein, Jill M ^a,b   Woo, Tsung Ung ^c   Petryshen, Tracey L ^d,e   Mesholam Gately, Raquelle I ^b   McCarley, Robert W ^b,f   Kikinis, Ron ^a   Shenton, Martha E ^a,f   Kubicki, Marek ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MCLEAN HOSPITAL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

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

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN MAPPING; CLINICAL ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DIFFUSION WEIGHTED IMAGING; EXTRACELLULAR SPACE; FEMALE; GRAY MATTER; HUMAN; MALE; NERVE FIBER DEGENERATION; NERVOUS SYSTEM INFLAMMATION; PRIORITY JOURNAL; PSYCHOSIS; SCHIZOPHRENIA; WHITE MATTER;

ADOLESCENT; ADULT; BRAIN; BRAIN MAPPING; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HUMANS; MALE; NERVE DEGENERATION; NERVE FIBERS, MYELINATED; PSYCHOTIC DISORDERS; SCHIZOPHRENIA;

EID: 84870160951     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2904-12.2012     Document Type: Article

References (58)

1. Acosta-Cabronero J, Williams GB, Pengas G, Nestor PJ (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. Brain 133:529-539.
2. Aja-Fernandez S, Niethammer M, Kubicki M, Shenton ME, Westin CF (2008) Restoration of DWI data using a Rician LMMSE estimator. IEEE Trans Med Imaging 27:1389-1403.
3. Alexander AL, Lee JE, Lazar M, Field AS (2007) Diffusion tensor imaging of the brain. Neurotherapeutics 4:316-329.
4. Andreasen NC (2010) The lifetime trajectory of schizophrenia and the concept of neurodevelopment. Dialogues Clin Neurosci 12:409-415.
5. Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34:51-61.
6. Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209-219.
7. Baumgartner C, Pasternak O, Bouix S, Westin C-F, Rathi Y (2012) Filtered multi-tensor tractography using free water estimation. Paper presented at International Society for Magnetic Resonance in Medicine Meeting, May 2012, Melbourne, Australia.
8. Cerqueira JJ, Pêgo JM, Taipa R, Bessa JM, Almeida OF, Sousa N (2005) Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 25:7792-7800.
9. Cloak CC, Chang L, Ernst T (2004) Increased frontal white matter diffusion is associated with glial metabolites and psychomotor slowing in HIV. J Neuroimmunol 157:147-152.
10. Connor CM, Crawford BC, Akbarian S (2011) White matter neuron alterations in schizophrenia and related disorders. Int J Dev Neurosci 29:325- 334.
11. Davis KL, Stewart DG, Friedman JI, Buchsbaum M, Harvey PD, Hof PR, Buxbaum J, Haroutunian V (2003) White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch Gen Psychiatry 60:443-456.
12. DeLisi LE, Szulc KU, Bertisch H, Majcher M, Brown K, Bappal A, Branch CA, Ardekani BA (2006) Early detection of schizophrenia by diffusion weighted imaging. Psychiatry Res 148:61-66.
13. Doorduin J, de Vries EF, Willemsen AT, de Groot JC, Dierckx RA, Klein HC (2009) Neuroinflammation in schizophrenia-related psychosis: a PET study. J Nucl Med 50:1801-1807.
14. Douaud G, Smith S, Jenkinson M, Behrens T, Johansen-Berg H, Vickers J, James S, Voets N, Watkins K, Matthews PM, James A (2007) Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain 130:2375-2386.
15. Ellison-Wright I, Bullmore E (2009) Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 108:3-10.
16. Garver DL, Holcomb JA, Christensen JD (2008) Compromised myelin integrity during psychosis with repair during remission in drug-responding schizophrenia. Int J Neuropsychopharmacol 11:49-61.
17. Gur Y, Pasternak O, Sochen N (2009) Fast GL (n)-invariant framework for tensors regularization. Int J Comp Vis 85:211-222.
18. Konrad A, Winterer G (2008) Disturbed structural connectivity in schizophrenia primary factor in pathology or epiphenomenon? Schizophr Bull 34:72-92.
19. Kubicki M, Shenton ME (2009) Diffusion tensor imaging and its application to schizophrenia and related disorders. Diffusion MRI: from quantitative measurement to in vivo neuroanatomy (Johansen-Berg H, Behrens T, eds). London, Academic.
20. Kubicki M, Park H, Westin CF, Nestor PG, Mulkern RV, Maier SE, Niznik-iewicz M, Connor EE, Levitt JJ, Frumin M, Kikinis R, Jolesz FA, McCarley RW, Shenton ME (2005) DTI and MTR abnormalities inschizophrenia: analysis of white matter integrity. Neuroimage 26:1109-1118.
21. Kubicki M, McCarley R, Westin CF, Park HJ, Maier S, Kikinis R, Jolesz FA, Shenton ME (2007) A review of diffusion tensor imaging studies in schizophrenia. J Psychiatr Res 41:15-30.
22. Kyriakopoulos M, Frangou S (2009) Recent diffusion tensor imaging findings in early stages of schizophrenia. Curr Opin Psychiatry 22:168-176.
23. Laan W, Smeets H, de Wit NJ, Kahn RS, Grobbee DE, Burger H (2009) Glucocorticosteroids associated with a decreased risk of psychosis. J Clin Psychopharmacol 29:288-290.
24. Lieberman JA (1999) Isschizophreniaa neurodegenerative disorder?Aclin-ical and neurobiological perspective. Biol Psychiatry 46:729-739.
25. Ling J, Merideth F, Caprihan A, Pena A, Teshiba T, Mayer AR (2012) Head injury or head motion? Assessment and quantification of motion artifacts in diffusion tensor imaging studies. Hum Brain Mapp 33:50-62.
26. Metzler-Baddeley C, Jones DK, Belaroussi B, Aggleton JP, O'Sullivan MJ (2011) Frontotemporal connections in episodic memory and aging: a diffusion MRI tractography study. J Neurosci 31:13236-13245.
27. Metzler-Baddeley C, O'Sullivan MJ, Bells S, Pasternak O, Jones DK (2012) How and how not to correct for CSF-contamination in diffusion MRI. Neuroimage 59:1394-1403.
28. Muller N, Schwarz M (2006) Schizophrenia as an inflammation-mediated dysbalance of glutamatergic neurotransmission. Neurotox Res 10:131-148.
29. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1-25.
30. Pantazopoulos H, Woo TU, Lim MP, Lange N, Berretta S (2010) Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia. Arch Gen Psychiatry 67:155-166.
31. Pasternak O, Sochen N, Gur Y, Intrator N, Assaf Y (2009) Free water elim-ination and mapping from diffusion MRI. Magn Reson Med 62:717-730.
32. Pasternak O, Sochen N, Basser PJ (2010) The effect of metric selection on the analysis of diffusion tensor MRI data. Neuroimage 49:2190-2204.
33. Pasternak O, Shenton ME, Westin CF (2012) Estimation of extracellular volume from regularized multi-shell diffusion MRI. Med Image Comput Comput Assist Interv LNCS 7511:305-312.
34. Peters BD, Blaas J, Haan LD (2010) Diffusion tensor imaging in the early phase of schizophrenia: what have we learned? J Psychiatr Res 44:993-1004.
35. Pfefferbaum A, Sullivan EV, Hedehus M, Moseley M, Lim KO (1999) Brain gray and white matter transverse relaxation time in schizophrenia. Psychiatry Res 91:93-100.
36. Pierpaoli C, Jones DK (2004) Removing CSF contamination in brain DT-MRIs by using a two-compartment tensor model. Paper presented at International Society for Magnetic Resonance in Medicine Meeting, May 2004, Kyoto, Japan.
37. Potvin S, Stip E, Sepehry AA, Gendron A, Bah R, Kouassi E (2008) Inflammatory cytokine alterations in schizophrenia: a systematic quantitative review. Biol Psychiatry 63:801-808.
38. Schwartz M, Butovsky O, Brück W, Hanisch UK (2006) Microglial pheno-type: is the commitment reversible? Trends Neurosci 29:68-74.
39. Segal D, Schmitz C, Hof PR (2009) Spatial distribution and density of oli-godendrocytes in the cingulum bundle are unaltered in schizophrenia. Acta Neuropathol 117:385-394.
40. Selemon LD, Kleinman JE, Herman MM, Goldman-Rakic PS (2002) Smaller Frontal Gray Matter Volume in Postmortem Schizophrenic Brains. Am J Psychiatry 159:1983-1991.
41. Selemon LD, Mrzljak J, Kleinman JE, Herman MM, Goldman-Rakic PS (2003) Regional specificity in the neuropathologic substrates of schizophrenia: a morphometric analysis of Broca's area 44 and area 9. Arch Gen Psychiatry 60:69-77.
42. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:83-98.
43. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487-1505.
44. Sommer IE, de Witte L, Begemann M, Kahn RS (2012) Nonsteroidal anti-inflammatory drugs in schizophrenia: ready for practiceoragood start? A meta-analysis. J Clin Psychiatry 73:414-419.
45. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH (2003) Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 20:1714-1722.
46. Steiner J, Bielau H, Brisch R, Danos P, Ullrich O, Mawrin C, Bernstein HG, Bogerts B (2008) Immunological aspects in the neurobiology of suicide: elevated microglial density in schizophrenia and depression is associated with suicide. J Psychiatr Res 42:151-157.
47. Streit WJ (2006) Microglial senescence: does the brain's immune system have an expiration date? Trends Neurosci 29:506-510.
48. Streit WJ, Mrak RE, Griffin WS (2004) Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 1:14.
49. Syková E, Nicholson C (2008) Diffusionin brain extracellular space. Physiol Rev 88:1277-1340.
50. Tamnes CK, Ostby Y, Fjell AM, Westlye LT, Due-Tonnessen P, Walhovd KB (2010) Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. Cereb Cortex 20:534-548.
51. Uranova NA, Vostrikov VM, Vikhreva OV, Zimina IS, Kolomeets NS, Orlo-vskaya DD (2007) The role of oligodendrocyte pathology in schizophrenia. Int J Neuropsychopharmacol 10:537-545.
52. van Berckel BN, Bossong MG, Boellaard R, Kloet R, Schuitemaker A, Caspers E, Luurtsema G, Windhorst AD, Cahn W, Lammertsma AA, Kahn RS (2008) Microglia activation inrecent-onset schizophrenia:a quantitative (R)-[11C]PK11195 positron emission tomography study. Biol Psychiatry 64:820-822.
53. Ventura J, Nuechterlein KH, Subotnik KL, Gutkind D, Gilbert EA (2000) Symptom dimensions in recent-onset schizophrenia and mania: a prin-cipal components analysis of the 24-item Brief Psychiatric Rating Scale. Psychiatry Res 97:129-135.
54. Wang Y, Wang Q, Haldar JP, Yeh FC, Xie M, Sun P, Tu TW, Trinkaus K, Klein
55. Song SK (2011) Quantification of increased cellularity during inflammatory demyelination. Brain 134:3590-3601.
56. Weiner HL, Selkoe DJ (2002) Inflammation and therapeutic vaccination in CNS diseases. Nature 420:879-884.
57. Whitford TJ, Grieve SM, Farrow TF, Gomes L, Brennan J, Harris AW, Gordon E, Williams LM (2006) Progressive grey matter atrophy over the first 2-3 years of illness in first-episode schizophrenia: a tensor-based morphometry study. Neuroimage 32:511-519.
58. Wuerfel J, Haertle M, Waiczies H, Tysiak E, Bechmann I, Wernecke KD, Zipp F, Paul F (2008) Perivascular spaces-MRI marker of inflammatory activity in the brain? Brain 131:2332-2340.