Relationship between exploratory eye movements and brain morphology in schizophrenia spectrum patients

Springer Science and Business Media LLC - Tập 255 - Trang 104-110 - 2004
M. Tsunoda1, Y. Kawasaki1, M. Matsui2, Y. Tonoya1, H. Hagino1, M. Suzuki1, H. Seto3, M. Kurachi1
1Department of Neuropsychiatry, Toyama Medical and Pharmaceutical University, Toyama 930-0194, Japan
2Department of Psychology, Toyama Medical and Pharmaceutical University, Toyama 930-0194, Japan
3Department of Radiology, Toyama Medical and Pharmaceutical University, Toyama 930-0194, Japan

Tóm tắt

The exploratory eye movements of schizophrenia patients and their relatives have been shown to differ from those of patients without schizophrenia and healthy controls. However the mechanism of exploratory eye movement disturbances in schizophrenia patients remains elusive. We investigated the relationship between the exploratory eye movements and brain morphology in 39 schizophrenia spectrum patients. Voxel–based morphometric analysis on three–dimensional magnetic resonance imaging was conducted by means of statistical parametric mapping 99. The decrease in the responsive search score, which is the total number of sections on which the eyes fixed in response to questioning in a comparison task, was significantly correlated with the decreased gray matter in the right frontal eye field (rFEF) including the right supplementary eye field (rSEF), right parietal eye field (rPEF), and right inferior frontal region. These results suggest that disturbance in exploratory eye movement in schizophrenia spectrum patients may be related to neural network dysfunction in FEF, SEF and PEF, which are the eye movement related areas, and in the inferior frontal region that may be related to information organization.

Tài liệu tham khảo

Andersen RA, Gnadt JW (1989) Posterior parietal cortex. In: Wurtz H,Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 315–336 Ashburner J, Friston K (1997) Multimodal image coregistration and partitioning: a unified framework. Neuroimage 6:209–217 Ashburner J, Friston KJ (2000) Voxel-based morphometry – The methods. Neuroimage 11:805–821 Baron M, Risch N (1987) The spectrum concept of schizophrenia: evidence for a genetic-environmental continuum. J Psychiatric Res 21:257–267 Benes FM, NcSparren J, Bird ED, SanGiovanni JP, Vincent SL (1991) Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 48:996–1001 Buchanan RW, Vladar K, Barta PE, Pearlson GD (1998) Structural evaluation of the prefrontal cortex in schizophrenia. Am J Psychiatry 155:1049–1055 Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA, Linenweber MR, Petersen SE, Raichle ME, Van Essen DC, Shulman GL (1998) A common network of functional areas for attention and eye movements. Neuron 21:761–773 Dickey CC, McCarley RW, Shenton ME (2002) The brain in schizotypal personality disorder: a review of structural MRI and CT findings. Harvard Rev Psychiatry 10:1–15 Diefendorf AR, Dogde R (1908) An experimental study of the ocular reactions of the insane from photographic records. Brain 31:451–489 First MB, Spitzer RL,Williams JBW, Gibson M (1996) Structured Clinical Interview for DSM-IV axis II disorders. New York State Psychiatric Institute, New York Fletcher PC, Shallice T, Dolan RJ (1998) The functional roles of prefrontal cortex in episodic memory I. Encoding. Brain 121:1239–1248 Friston KJ, Frith CD, Liddle PF, Dolan RJ, Lammertsma AA, Frackowiak, RSJ (1990) The relationship between global and local changes in PET scans. J Cereb Blood Flow Metab 10:458–466 Gaymard B, Ploner CJ, Rivaud S, Vermersch AI, Pierrot-Deseilligny C (1998) Cortical control of saccades. Exp Brain Res 123:159–163 Goldberg ME, Segraves MA (1989) The visual and frontal cortices. In: Wurtz RH,Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 283–314 Hagino H, Suzuki M, Mori K, Nohara S, Yamashita I, Takahashi T, Kurokawa K, Matsui M, Watanabe N, Seto H, Kurachi M (2002) Proton magnetic resonance spectroscopy of the inferior frontal gyrus and thalamus and its relationship to verbal learning task performance in patients with schizophrenia: a preliminary report. Psychiatry Clin Neurosci 56:499–507 Heide W, Kompf D (1998) Combined deficits of saccades and visuo- spatial orientation after cortical lesions. Exp Brain Res 123:164–171 Holzman PS, Proctor LR, Hughes DW (1973) Eye tracking patterns in schizophrenia. Science 181:179–181 Kendler KS, Masterson CC, Urgaro R, Davis KL (1984) A family history study of schizophrenia-related personality disorders. Am J Psychiatry 141:424–427 Kawasaki Y, Suzuki M, Nohara S, Hagino H, Takahashi T, Matsui M, Yamashita I, Chitnis XA, McGuire PK, Seto H, Kurachi M (2004) Structural brain differences in patients with schizophrenia and schizotypal disorder demonstrated by voxel-based morphometry. Eur Arch Psychiatry Clin Neurosci (in press) Kendler KS, Neale MC, Walsh D (1995) Evaluating the spectrum concept of schizophrenia in the Roscommon family study. Am J Psychiatry 152:749–754 Kojima T, Matsushima E, Nakajima K, Shiraishi H, Ando K, Ando H, Shimazono Y (1990) Eye movements in acute, chronic and remitted schizophrenics. Biol Psychiatry 27:975–989 Kojima T, Matsushima E, Ando K, Ando H (1992) Exploratory eye movements and neuropsychological tests in schizophrenic patients. Schizophr Bull 18:85–94 Kojima T, Matsushima E, Ando K (eds) (2000) Eyes and the mind. Japan Scientific Societies Press and S Karger, Tokyo Basel Kojima T, Matsushima E, Ohta K, Toru M (2001) Stability of exploratory eye movements as a marker of schizophrenia – a WHO multi-center study. Schizophr Res 52:203–213 Kurachi M, Matsui M, Kiba K, Suzuki M, Tsunoda M, Yamaguchi N, (1994) Limited visual search on the WAIS picture completion test in patients with schizophrenia. Schizophr Res 12:75–80 Lawrie SM, Abukmeil SS (1998) Brain abnormality in schizophrenia: a systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry 172:110–120 Lawrie SM, Whalley H, Kestelman JN, Abukmeil SS, Byrne M, Hodges A, Rimmington JE, Best JJ, Owens DG, Johnstone EC (1999) Magnetic resonance imaging of brain in people at high risk of developing schizophrenia. Lancet 353:30–33 Lawrie SM, Whalley HC, Abukmeil SS, Kestelman JN, Donnelly L, Miller P, Best JJK, Owens BDGC, Johnstone EC (2001) Brain structure, genetic liability, and psychotic symptoms in subjects at high risk of developing schizophrenia. Biol Psychiatry 49:811–823 Matsushima E, Kojima T, Ohbayashi S, Ando H, Ando K, Shimazono Y (1992) Exploratory eye movements in schizophrenic patients and patients with frontal lobe lesions. Eur Arch Psychiatry Clin Neurosci 241:310–314 Matsushima E, Takebayashi H, Kojima T (1996) Abnormalexploratory eye movements and cognitive mechanism in patients with schizophrenia. Rinsho Noha (Clinical Electroencephalography) 38:291–294 (in Japanese) Matsushima E, Kojima T, Ohta K, Obayashi S, Nakajima K, Kakuma T, Ando H, Toru M (1998) Exploratory eye movement dysfunctions in patients with schizophrenia: possibility as a discriminator for schizophrenia. J Psychiatr Res 32:289–295 Matsushima E, Kubo H, Kojima T, Ohta K (1999) Exploratory eye movement in patients with schizophrenia – a monozygotic twins study. In: Abstracts II of the XI World Congress of Psychiatry, Hamburg, p 11 Moriya H, Ando K,Kojima T, Shimazono Y, Ogiwara R, Jimbo K, Ushikubo T (1972) Eye movements during perception of pictures I chronic schizophrenia. Folia Psychiat Neurol Jpn 26:189–199 Nohara S, Suzuki M, Kurachi M, Yamashita I, Masui M, Seto H, Saitoh O (2000) Neural correlates of memory organization deficits schizophrenia – A single photon emission computed tomography study with 99m Tc-ECD during a verbal learning task. Schizophr Res 42:209–222 Pierrot-Deseilligny C, Rivaud S, Gaymard B, Muri R, Vermersch AI (1995) Cortical control of saccades. Ann Neurol 37:557–567 Pierrot-Deseilligny C, Gaymard B, Muri R, Rivaud S (1997) Cerebral ocular motor sign. J Neurol 244:65–70 Schlaepfer TE, Harris GJ, Tien AY, Peng LW, Lee S, Federman EB, Chase GA, Barta PE, Pearlson GD (1994) Decreased regional cortical gray matter volume in schizophrenia. Am J Psychiatry 151:842–848 Seidman LJ, Faraone SV, Goldstein JM, Kremen WS, Horton NJ, Makris N, Toomey R, Kennedy D, Caviness VS, Tsuang MT (2002) Left hippocampal volume as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric study of nonpsychotic first-degree relatives. Arch Gen Psychiatry 59:839–849 Selemon LD, Rajkowska G, Goldman-Rakic PS (1995) Abnormally high neuronal density in the schizophrenic cortex. Arch Gen Psychiatry 52:805–818 Shagass C, Roemer RA, Amadeo M (1976) Eye-tracking performance and engagement of attention. Arch Gen Psychiatry 33:121–125 Shenton ME, Dickey CC, Frumin M, McCarley RW (2001) A review of MRI findings in schizophrenia. Schizophr Res 49:1–52 Siever LJ, Koeningsberg HW, Harvey P, Mitropoulou V, Laruelle M, Abi-Dargham A, Goodman M, Buchsbaum M (2002) Cognitive and brain function in schizotypal personality disorder. Schizophr Res 54:157–167 Suzuki M, Nohara S, Hagino H, Kurokawa K, Yotsutsuji T, Kasasaki Y, Takahashi T, Matsui M, Watanabe N, Seto H, Kurachi M (2002) Regional changes in brain gray and white matter in patients with schizophrenia demonstrated with voxel-based analysis of MRI. Schizophr Res 55:41–54 Takahashi S, Tanabe E, Sakai T, Xia M, Matsuura M, Matsushima E, Obayashi S, Kojima T (1996) Correlation between neurophysiological abnormalities and brain morphological changes in schizophrenia. Rinsho Noha (Clinical Electroencephalography) 38:85–91 (in Japanese) Takahashi S, Tanabe E, Kojima T, Matsushima E, Yara K (1999) Exploratory eye movement of dysfunction in schizophrenic patients and their siblings. In: Abstracts II of the XI World Congress of Psychiatry, Hamburg, p 15 Takahashi T, Suzuki M, Kawasaki Y, Kurokawa K, Hagino H, Yamashita I, Zhou S-Y, Nohara S, Nakamura K, Seto H, Kurachi M (2002) Volumetric magnetic resonance imaging study of the anterior cingulate gyrus in schizotypal disorder. Eur Arch Psychiatry Clin Neurosci 252:268–277 Talairach J, Tournoux P (1998) Co-planar stereotaxic atlas of the human brain. Georg Thieme, Stuttgart-New York Tonoya Y, Matsui M, Kurachi M, Kurokawa K, Sumiyoshi T (2002) Exploratory eye movements in schizophrenia: effects of figure size and the instruction on visual search. Eur Arch Psychiatry Clin Neurosci 252:255–261 Tsuang MT, Bucher KD, Fleming JA (1983) A search for ‘schizophrenia spectrum disorders’. An application of a multiple threshold model to blind family study data. Br J Psychiatry 143:572–577 Tsunoda M, Kurachi M, Yuasa S, Kadono Y, Matsui M, Shimizu A, (1992) Scanning eye movements in schizophrenic patients: relationship to clinical symptoms and regional cerebral blood flow using 123I-IMP SPECT. Schizophr Res 7:159–168 Van Erp TG, Saleh PA, Rosso IM, Huttunen M, Lonnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen VP, Standerskjold- Nordenstam CG, Cannon TD (2002) Contributions of genetic risk and fetal hypoxia to hippocampal volume in patients with schizophrenia or schizoaffective disorder, their unaffected siblings, and healthy unrelated volunteers. Am J Psychiatry 159:1514–1520 Wing JK, Cooper JE, Sartorius N (1974) Measurement and classification of psychiatric symptoms.An introduction manual for the PSE and CATEGO program. Cambridge University Press, London World Health Organization (1993) The ICD-10 Classification of Mental and Behavioural Disorders: Diagnostic Criteria for Research. World Health Organization, Geneva Wright IC, Ellison ZR, Sharma T, Friston KJ, Murray RM, McGuire PK (1999) Mapping of grey matter changes in schizophrenia. Schizophr Res 35:1–14 Wright IC, Rabe-Hesketh S, Woodruff PWR, David AS, Murray RM, Bullmore ET (2000) Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 157:16–25 Xia ML, Takahashi S, Tanabe E, Matsushima M, Kojima T, Matsushima E (1996) Eye movement studies on schizophrenics and their parents. Eur Neuropsychopharm 6(Suppl 3):64 Yoneyama E, Matsui M, Kawasaki Y, Nohara S, Takahashi T, Hagino H, Suzuki M, Seto H, Kurachi M (2003) Gray matter features of schizotypal disorder patients exhibiting the schizophrenia- related code types of the Minnesota Multiphasic Personality Inventory. Acta Psychiatr Scand 108:333–340 Zipursky RB, Lim KO, Sullivan EV, Brown BW, Pfefferbaum A (1992) Widespread cerebral gray matter volume deficits in schizophrenia. Arch Gen Psychiatry 49:195–205