Neuropathological abnormalities in schizophrenia: Evidence from magnetization transfer imaging

Brain

Volumn 124, Issue 5, 2001, Pages 882-892

  Foong, J ^a,d   Symms, M R ^a   Barker, G J ^a   Maier, M ^b   Woermann, F G ^c   Miller, D H ^a   Ron, M A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^c EPILEPSY CENTER BETHEL   (Germany)

^d NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

Author keywords

Magnetization transfer imaging; Magnetization transfer ratio; Neuropathological abnormalities; Schizophrenia

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS CALLOSUM; DISEASE SEVERITY; FEMALE; FRONTAL LOBE; HUMAN; MALE; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PARIETAL LOBE; PRIORITY JOURNAL; SCHIZOPHRENIA; TEMPORAL LOBE;

EID: 0035005652     PISSN: 00068950     EISSN: None     Source Type: Journal    
DOI: 10.1093/brain/124.5.882     Document Type: Article

References (76)

1. Akbarian S, Vinuela A, Kim JJ, Potkin SG, Bunney WE Jr, Jones EG. Distorted distribution of nicotinamide-adenine dinucleotide phosphate-diaphorase neurons in temporal lobe of schizophrenics implies anomalous cortical development. Arch Gen Psychiatry 1993; 50: 178-87.
2. Annett MA. A classification of hand preference by association analysis. Br J Psychol 1970; 61: 303-21.
3. Arnold SE, Lee VM-Y, Gur RE, Trojanowski JQ. Abnormal expression of two microtubule-associated proteins (MAP2 and MAP5) in specific subfields of the hippocampal formation in schizophrenia. Proc Natl Acad Sci USA 1991; 88: 10850-4.
4. Ashburner J, Friston KJ. Voxel-based morphometry - the methods. [Review]. Neuroimage 2000; 11: 805-21.
5. Baare WF, Hulshoff Pol HE, Hijman R, Mali WP, Viergever MA, Kahn RS. Volumetric analysis of frontal lobe regions in schizophrenia: relation to cognitive function and symptomatology. Biol Psychiatry 1999; 45: 1597-605.
6. Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL. Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 1991; 48: 996-1001.
7. Benes FM, Kwok EW, Vincent SL, Todtenkopf MS. A reduction of non-pyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry 1998; 44: 88-97.
8. Bertolino A, Nawroz S, Mattay VS, Barnett AS, Duyn JH, Moonen CT, et al. Regionally specific pattern of neurochemical pathology in schizophrenia as assessed by multislice proton magnetic resonance spectroscopic imaging. Am J Psychiatry 1996; 153: 1554-63.
9. Bogerts B, Falkai P, Haupts M, Greve B, Ernst S, Tapernon-Franz U, et al. Post-mortem volume measurements of limbic system and basal ganglia structures in chronic schizophrenics. Initial results from a new brain collection. Schizophr Res 1990; 3: 295-301.
10. Breier A, Buchanan RW, Elkashef A, Munson RC, Kirkpatrick B, Gellad F. Brain morphology and schizophrenia. A magnetic resonance imaging study of limbic, prefrontal cortex and caudate structures. Arch Gen Psychiatry 1992; 49: 921-6.
11. Buchsbaum MS, Tang CY, Peled S, Gudbjartsson H, Lu D, Hazlett EA, et al. MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia. Neuroreport 1998; 9: 425-30.
12. Cotter D, Wilson S, Roberts E, Kerwin R, Everall IP. Increased dendritic MAP2 expression in the hippocampus in schizophrenia. Schizophr Res 2000; 41: 313-23.
13. de Courten-Myers GM. The human cerebral cortex: gender differences in structure and function. J Neuropathol Exp Neurol 1999; 58: 217-26.
14. Dousset V, Grossman RI, Ramer KN, Schnall MD, Young LH, Gonzalez-Scarano F, et al. Experimental allergic encephalomyelitis and multiple sclerosis: lesion characterization with magnetization transfer imaging. Radiology 1992; 182: 483-91.
15. Dousset V, Armand JP, Lacoste D, Mieze S, Letenneur L, Dartigues JF, et al. Magnetization transfer study of HIV encephalitis and progressive multifocal leukoencephalopathy. AJNR Am J Neuroradiol 1997; 18: 895-901.
16. Falkai P, Bogerts B, Rozumek M. Limbic pathology in schizophrenia: the entorhinal region - a morphometric study. Biol Psychiatry 1988; 24: 515-21.
17. Filippi M, Campi A, Dousset V, Baratti C, Martinelli V, Canal N, et al. A magnetization transfer imaging study of normal appearing white matter in multiple sclerosis. Neurology 1995; 45: 478-82.
18. Foong J, Maier M, Barker GJ, Brocklehurst S, Miller DH, Ron MA. In vivo investigation of white matter pathology in schizophrenia with magnetization transfer imaging. J Neurol Neurosurg Psychiatry 2000; 68: 70-4.
19. Friston KJ, Ashburner J, Frith CD, Poline JB, Heather JD, Frackowiak RS. Spatial registration and normalization of images. Hum Brain Mapp 1995a; 3: 165-89.
20. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RS. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 1995b; 2: 189-10.
21. Frith CD, Friston KJ, Herold S, Silbersweig D, Fletcher P, Cahill C, et al. Regional brain activity in chronic schizophrenic patients during the performance of a verbal fluency task. Br J Psychiatry 1995; 167: 343-9.
22. Gass A, Barker GJ, Kidd D, Thorpe JW, MacManus DG, Brennan A, et al. Correlation of magnetization transfer ratio and clinical disability in multiple sclerosis. Ann Neurol 1994; 36: 62-7.
23. Glantz LA, Lewis DA. Reduction of synaptophysin immunoreactivity in the prefrontal cortex of subjects with schizophrenia: regional and diagnostic specificity. Arch Gen Psychiatry 1997; 54: 943-52.
24. Glantz LA, Lewis DA. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 2000; 57: 65-73.
25. Goldstein JM, Goodman JM, Seidman LJ, Kennedy DN, Makris N, Lee H, et al. Cortical abnormalities in schizophrenia identified by structural magnetic resonance imaging. Arch Gen Psychiatry 1999; 56: 537-47.
26. Goldthorpe JH, Hope K. The social grading of occupations: a new approach and scale. Oxford: Clarendon Press; 1974.
27. Gunther W, Petsch R, Steinberg R, Moser E, Streck P, Heller H, et al. Brain dysfunction during motor activation and corpus callosum alterations in schizophrenia measured by cerebral blood flow and magnetic resonance imaging. Biol Psychiatry 1991; 29: 535-55.
28. Harrison PJ. The neuropathological effects of antipsychotic drugs. [Review]. Schizophr Res 1999; 40: 87-99.
29. Harrison PJ, Eastwood SL. Preferential involvement of excitatory neurons in medial temporal lobe in schizophrenia. Lancet 1998; 352: 1669-73.
30. Harvey I, Ron MA, Du Boulay G, Wicks D, Lewis SW, Murray RM. Reduction of cortical volume in schizophrenia on magnetic resonance imaging. [Review]. Psychol Med 1993; 23: 591-604.
31. Jonsson SA, Luts A, Guldberg-Kjaer N, Brun A. Hippocampal pyramidal cell disarray correlates negatively to cell number: implications for the pathogenesis of schizophrenia. Eur Arch Psychiatry Clin Neurosci 1997; 247: 120-7.
32. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 1987; 13: 261-76.
33. Lawrie SM, Abukmeil SS. Brain abnormality in schizophrenia. A systematic and quantitative review of volumetric magnetic resonance imaging studies. [Review]. Br J Psychiatry 1998; 172: 110-20.
34. Lim KO, Sullivan EV, Zipursky RB, Pfefferbaum A. Cortical gray matter volume deficits in schizophrenia: a replication. Schizophr Res 1996; 20: 157-64.
35. Lim KO, Adalsteinsson E, Spielman D, Sullivan EV, Rosenbloom MJ, Pfefferbaum A. Proton magnetic resonance spectroscopic imaging of cortical gray and white matter in schizophrenia. Arch Gen Psychiatry 1998; 55: 346-52.
36. Lim KO, Hedehus M, Moseley M, de Crespigny A, Sullivan EV, Pfefferbaum A. Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry 1999; 56: 367-74.
37. Maier M, Ron MA, Barker GJ, Tofts PS. Proton magnetic resonance spectroscopy: an in vivo method of estimating hippocampal neuronal depletion in schizophrenia. Psychol Med 1995; 25: 1201-9.
38. Marsh L, Suddath RL, Higgins N, Weinberger DR. Medial temporal lobe structures in schizophrenia: relationship of size to duration of illness. Schizophr Res 1994; 11: 225-38.
39. McGuire PK, Frith CD. Disordered functional connectivity in schizophrenia [editorial]. Psychol Med 1996; 26: 663-7.
40. Mottershead JP, Thornton JS, Clemence M, Scaravilli F, Newcombe J, Cuzner ML, et al. Correlation of spinal cord axonal density with post mortem NMR measurements in multiple sclerosis and controls [abstract]. Proceedings of International Society for Magnetic Resonance in Medicine 6th meeting 1998. p. 2163.
41. Nelson H, Willison J. National Adult Reading Test (NART). 2nd edn. Windsor (UK): NFER-Nelson; 1991.
42. Pakkenberg B. Post-mortem study of chronic schizophrenic brains. Br J Psychiatry 1987; 151: 744-52.
43. Pakkenberg B. Total nerve cell number in neocortex in chronic schizophrenics and controls estimated using optical disectors. Biol Psychiatry 1993; 34: 768-72.
44. Pearlson GD, Barta PE, Powers RE, Menon RR, Richards SS, Aylward EH, et al. Medial and superior temporal gyral volumes and cerebral asymmetry in schizophrenia versus bipolar disorder. Biol Psychiatry 1997; 41: 1-14.
45. Perrone-Bizzozero NI, Sower AC, Bird ED, Benowitz LI, Ivins KJ, Neve RL. Levels of the growth-associated protein GAP-43 are selectively increased in association cortices in schizophrenia. Proc Natl Acad Sci USA 1996; 93: 14182-7.
46. Portas CM, Goldstein JM, Shenton ME, Hokama HH, Wible CG, Fischer I, et al. Volumetric evaluation of the thalamus in schizophrenic male patients using magnetic resonance imaging. Biol Psychiatry 1998; 43: 649-59.
47. Rabinowicz T, Dean DE, Petetot JM, de Courten-Myers GM. Gender differences in the human cerebral cortex: more neurons in males; more processes in females. J Child Neurol 1999; 14: 98-107.
48. Rajkowska G, Selemon LD, Goldman-Rakic PS. Neuronal and glial somal size in the prefrontal cortex. Arch Gen Psychiatry 1998; 55: 215-24.
49. Renshaw PF, Yurgelun-Todd DA, Toben M, Gruber SA, Cohen BM. Temporal lobe proton magnetic resonance spectroscopy of patients with first episode psychosis. Am J Psychiatry 1995; 152: 444-6.
50. Rosoklija G, Toomayan G, Ellis SP, Keilp J, Mann JJ, Latov N, et al. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders. Arch Gen Psychiatry 2000; 57: 349-56.
51. Sanfilipo M, Lafargue T, Rusinek H, Arena L, Loneragan C, Lautin A, et al. Volumetric measure of the frontal and temporal lobe regions in schizophrenia. Relationship to negative symptoms. Arch Gen Psychiatry 2000; 57: 471-80.
52. Schlaepter TE, Harris GJ, Tien AY, Peng LW, Lee S, Federman EB, et al. Decreased regional cortical gray matter volume in schizophrenia. Am J Psychiatry 1994; 151: 842-8.
53. Selemon LD, Goldman-Rakic PS. The reduced neuropil hypothesis: a circuit based model of schizophrenia. [Review]. Biol Psychiatry 1999; 45: 17-25.
54. Selemon LD, Rajkowska G, Goldman-Rakic PS. Abnormally high neuronal density in the schizophrenic cortex. A morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 1995; 52: 805-18.
55. Selemon LD, Rajkowska G, Goldman-Rakic PS. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a three dimensional, stereologic counting method. J Comp Neurol 1998; 392: 402-12.
56. Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, et al. Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. N Engl J Med 1992; 327: 604-12.
57. Sigmundsson T, Suckling J, Maier M, Williams SCR, Bullmore ET, Greenwood K, et al. Structural abnormalities in frontal, temporal and limbic regions and interconnecting white matter tracts in schizophrenia. Am J Psych 2001; 158: 234-43.
58. Silver NC, Barker GJ, MacManus DG, Miller DH, Thorpe JW, Howard R. Decreased magnetisation transfer ratio due to demyelination: a case of central pontine myelinolysis [letter]. J Neurol Neurosurg Psychiatry 1996; 61: 208-9.
59. Silver NC, Barker GJ, MacManus DG, Tofts PS, Miller DH. Magnetisation transfer ratio of normal brain white matter: a normative database spanning four decades of life. J Neurol Neurosurg Psychiatry 1997; 62: 223-8.
60. Suddath RL, Christison GW, Torrey EF, Casanova MF, Weinberger DR. Anatomical abnormalities in the brains of monozygotic twins discordant for schizophrenia. N Engl J Med 1990; 322: 789-94.
61. Sullivan EV, Lim KO, Mathalon D, Marsh L, Beal DM, Harris D, et al. A profile of cortical gray matter volume deficits characteristic of schizophrenia. Cereb Cortex 1998; 8: 117-24.
62. Symms MR, Wang L, Barker GJ, Tofts PS. Detection of serial changes in transient ischaemic attack using image registration [abstract]. Proceedings of the International Society for Magnetic Resonance in Medicine 4th meeting. New York; 1996. p. 558.
63. Thorpe JW, Barker GJ, Jones SI, Moseley I, Losseff, MacManus DG, et al. Magnetisation transfer ratios and transverse magnetisation decay curves in optic neuritis; correlation with clinical findings and electrophysiology. J Neurol Neurosurg Psychiatry 1995; 59: 487-92.
64. Tibbo P, Nopoulos P, Arndt S, Andreason NC. Corpus callosum shape and size in male patients with schizophrenia. Biol Psychiatry 1998; 44: 405-12.
65. Van Waesberghe JH, van Walderveen MA, de Groot CJ, Ravid R, Lycklama a Nijeholt GJ, Kamphorst W, et al. Post mortem correlation between axonal loss, MTR and hypointensity on T1 SE in MS. Proceedings of the International Society for Magnetic Resonance in Medicine 6th meeting 1998. p. 1334.
66. Weinberger DR, Berman KF, Suddath RL, Torrey EF. Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. Am J Psychiatry 1992; 149: 890-7.
67. Woermann FG, Free SL, Koepp MJ, Ashburner J, Duncan JS. Voxel-by-voxel comparison of automatically segmented cerebral gray matter - a rater-independent comparison of structural MRI in patients with epilepsy. Neuroimage 1999; 10: 373-84.
68. Woodruff PW, Phillips ML, Rushe T, Wright IC, Murray RM, David AS. Corpus callosum size and inter-hemispheric function in schizophrenia. Schizophr Res 1997a; 23: 189-96.
69. Woodruff PW, Wright IC, Shuriquie N, Russouw H, Rushe T, Howard RJ, et al. Structural brain abnormalities in male schizophrenics reflect fronto-temporal dissociation. Psychol Med 1997b; 27: 1257-66.
70. Woods RP, Cherry SR, Mazziotta JC. Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 1992; 16: 620-33.
71. Wright IC, Sharma T, Ellison ZR, McGuire PK, Friston KJ, Brammer MJ, et al. Supra-regional brain systems and the neuropathology of schizophrenia. Cereb Cortex 1999; 9: 366-78.
72. Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, Bullmore ET. Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 2000; 157: 16-25.
73. Young CE, Arima K, Xie J, Hu L, Beach TG, Falkai P, et al. SNAP-25 deficit and hippocampal connectivity in schizophrenia. Cereb Cortex 1998; 8: 261-8.
74. Yurgelun-Todd DA, Renshaw PF, Gruber SA, Ed M, Waternaux C, Cohen BM. Proton magnetic resonance spectroscopy of the temporal lobes in schizophrenics and normal controls. Schizophr Res 1996; 19: 55-9.
75. Zaidel DW, Esiri MM, Harrison PJ. The hippocampus in schizophrenia: lateralized increase in neuronal density and altered cytoarchitectural asymmetry. Psychol Med 1997; 27: 703-13.
76. Zipursky RB, Lim KO, Sullivan EV, Brown BW, Pfefferbaum A. Widespread cerebral gray matter volume deficits in schizophrenia. Arch Gen Psychiatry 1992; 49: 195-205.