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Abnormal Angular Gyrus Asymmetry in Schizophrenia

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Abnormal Angular Gyrus Asymmetry in Schizophrenia Abnormal Angular Gyrus Asymmetry in Schizophrenia Margaret Niznikiewicz, Ph.D., Robert Donnino, A.B., Robert W. McCarley, M.D., Paul G. Nestor, Ph.D., Daniel V. Iosifescu, M.D., Brian O’Donnell, Ph.D., James Levitt, M.D., and Martha E. Shenton, Ph.D. Objective: Few studies have evaluated the parietal lobe in schizophrenia despite the fact that it has an important role in attention, memory, and language—all functions that have been reported to be abnormal in schizophrenia. The inferior parietal lobule, in particular, is of interest because it is not only part of the heteromodal association cortex but also is part of the semantic-lexical network, which also includes the planum temporale. Both the infe- rior parietal lobule, particularly the angular gyrus of the inferior parietal lobule, and the planum temporale are brain regions that play a critical role as biological substrates of lan- guage and thought. The authors compared volume and asymmetry measures of the indi- vidual gyri of the parietal lobe by means of magnetic resonance imaging (MRI) scans. Method: MRI scans with a 1.5-Tesla magnet were obtained from 15 male chronic schizo- phrenic and 15 comparison subjects matched for age, gender, and parental socioeconomic status. Results: Inferior parietal lobule volumes showed a leftward asymmetry (left 7.0% larger than right) in comparison subjects and a reversed asymmetry (left 6.3% smaller than right) in schizophrenic subjects. The angular gyrus accounted for this difference in asym- metry, with the left angular gyrus being significantly larger (18.7%) than the right in compar- ison subjects, a finding that was not observed in schizophrenic patients. A further test of angular gyrus asymmetry showed a reversal of the normal left-greater-than-right asymme- try in the schizophrenic patients. Conclusions: Patients with schizophrenia showed a re- versed asymmetry in the inferior parietal lobule that was localized to the angular gyrus, a structure belonging to the heteromodal association cortex as well as being part of the se- mantic-lexical network. This finding contributes to a more comprehensive understanding of the neural substrates of language and thought disorder in schizophrenia. (Am J Psychiatry 2000; 157:428–437) The parietal lobe has received little attention in of the brain is further highlighted by the fact that only schizophrenia despite its recognized importance in nine magnetic resonance imaging (MRI) studies of the processes that are likely disturbed in schizophrenia, parietal lobe, in contrast to more than 35 for both tem- such as language (1), spatial working memory, and at- poral and frontal lobes, have been conducted in sub- tention (2–4). This lack of attention to parietal regions jects with schizophrenia (5, 6). The parietal lobe itself consists of the postcentral gy- Received Feb. 8, 1999; revisions received June 28, Aug. 16, and rus, superior parietal gyrus, and inferior parietal lobule, Sept. 20, 1999; accepted Sept. 20, 1999. From the Laboratory of Neuroscience, Clinical Neuroscience Division, Department of Psy- which is further subdivided into the supramarginal gy- chiatry, VA Medical Center, Harvard Medical School; and the Surgi- rus (area 39) and angular gyrus (area 40). The inferior cal Planning Laboratory, MRI Division, Department of Radiology, parietal lobule is part of the heteromodal association Brigham and Women’s Hospital, Harvard Medical School, Boston. cortex, which has been proposed as the site of the key Address reprint requests to Dr. Shenton, Department of Psychiatry- abnormality in schizophrenia (7). Further, both the su- 116A, VA Medical Center, Harvard Medical School, 940 Belmont St., Brockton, MA 02301. pramarginal gyrus and the angular gyrus have been de- Supported by NIMH grants MH-50740 and MH-01110 (to Dr. scribed as part of a semantic-lexical network that sup- Shenton) and MH-40799 (to Dr. McCarley), and grants from the ports “word meanings” represented by a “grid of Department of Veterans Affairs Center for Clinical and Basic Neu- connectivity” that constitutes a “final pathway for the roscience Studies of Schizophrenia and a Department of Veterans Affairs Merit Application (Dr. McCarley). chunking of words into thought” (1). The role of the in- The authors thank Chris Dodd, B.A., Alaka Pellock, A.B., and ferior parietal lobule, and especially the angular gyrus, Marie Fairbanks for their administrative assistance. in language comprehension has been further confirmed 428 Am J Psychiatry 157:3, March 2000 NIZNIKIEWICZ, DONNINO, MCCARLEY, ET AL. by functional MRI (fMRI) and positron emission to- from the Schedule for Affective Disorders and Schizophrenia (26) and mography studies (8–10). Moreover, the semantic-lexi- from hospital chart reviews. All patients were receiving neuroleptic medication equivalent to a mean of 881 mg of chlorpromazine per cal network proposed by Mesulam (1) includes both the day. The patients had spent a mean of 7.1 years (SD=4.6) in the hos- inferior parietal lobule and the planum temporale, the pital, with a mean duration of illness of 15.8 years (SD=8.8). latter being located on the superioposterior surface of Fifteen normal comparison subjects were matched to the patient superior temporal gyrus, which, in turn, has been corre- group on gender (male), handedness (right), age (20–55 years, lated with symptoms of thought disorder (5, 6, 11). matched within 2 years), and parental socioeconomic status. No comparison subjects had a history of mental illness nor did their More anteriorly, the superior temporal gyrus has been first-degree relatives. The exclusion criteria for both groups in- correlated with auditory hallucinations (5, 6, 12). cluded no major drug or alcohol abuse in the previous 5 years, no Of note, the inferior parietal lobule and neighboring history of electroconvulsive therapy, no neurological illness, and no cortical regions often exhibit marked lateral asymmetry medications known to affect brain MRI scans (e.g., steroids). There (13, 14) and belong to structures that support lan- were no statistical differences between the comparison and schizo- phrenic subjects in height, weight, head circumference, or scores on guage. The presence of left-greater-than-right asymme- the WAIS-R information subscale (27). Written informed consent try also appears to be important for normal language was obtained from all 30 subjects after the procedures had been development. For example, the absence of normal later- fully explained. alization in these regions has been reported in subjects Clinical and Neuropsychological Measures with autism (15, 16) as well as in other language disor- ders (17). In schizophrenia, a reversal of normal asym- Eleven patients were categorized as having mostly positive symp- metry in the superior temporal gyrus, including the toms according to the Scale for the Assessment of Positive Symptoms planum temporale, has been associated with thought (28), none had mostly negative symptoms according to the Scale for disorder (5, 6). Thus, a reversal in normal asymmetry the Assessment of Negative Symptoms (29), and four were rated as having mixed negative and positive symptoms. The mean score on may be importantly related to schizophrenic pathology the Thought Disorder Index (30) for the patients was 60.4 (SD= (18–20). Consistent with these findings, we hypothe- 61.8), on which normal subjects score no greater than 5. Schizo- sized that a reversal of normal asymmetry in the supe- phrenic patients were evaluated by means of both standardized and rior temporal gyrus would also be found in the inferior experimental neuropsychological procedures (31). parietal lobule. Furthermore, since cortical asymme- MRI Methods tries are present during fetal development (21), finding an absence or a reversal of normal asymmetry might in- Image acquisition. A detailed description of the parcellation rules dicate a disruption in neuronal development. and anatomical definitions used in this study is included in appendix 1. The MRI images were acquired on a Signa 1.5-T system The relevance of the angular gyrus and supramar- (GE Medical Systems, Milwaukee). A sagittal localizer was used to ginal gyrus to schizophrenia stems not only from their orient the images in the proper plane. Total brain volume was ob- functions as part of the heteromodal association cortex tained by means of a double-echo, spin-echo acquisition with the fol- but also from their reciprocal neuroanatomical connec- lowing parameters: TR=3000 msec, TE=30 and 80 msec, field of × tions to the prefrontal (22) and temporal lobes (23)— view=24 cm, acquisition matrix=256 256 pixels, and voxel dimen- sions=0.9 mm × 0.9 mm × 3 mm, which resulted in 108 contiguous brain regions that have been shown to have disease-re- double-echo axial slices (54 levels). lated abnormalities. We examined these neuroanatomi- For the inferior parietal lobule brain regions, a three-dimensional cal relationships by capitalizing on the opportunity of Fourier transform spoiled gradient recall acquisition was used with having volumetric data on prefrontal and temporal the following parameters: TR=35 msec, TE=5 msec with one repeti- ° × × lobe regions in the same subjects (11, 24, 25). If the hy- tion, flip angle=45 ; field of view=24 cm; matrix=256 256 124 (192 phase-encoding steps). The dimensions for each voxel were 0.9 pothesis that schizophrenia is a disorder characterized mm × 0.9 mm × 1.5 mm. The images were reformatted into 124 con- primarily by heteromodal association cortex abnormal- tiguous 1.5-mm coronal slices. ities is correct, then higher correlations between the in- Image processing. Image processing was completed on worksta- ferior parietal lobule and other areas interconnected tions (Sun Microsystems, Mountain View, Calif.) with several multi- with the heteromodal association cortex would be pre- step computer algorithms. A postprocessing filter was used to reduce noise and to enhance morphologic details (32), followed by a semi- dicted for schizophrenic patients but not for compari- automated segmentation algorithm used to separate gray matter, son subjects.
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