Journal ofAffective Disorders, 21 (1991) 19-22 0 1991 Elsevier Science Publishers B.V. (Biomedical ADONIS 016503279100053D
19 Division)
0165-0327/91/$03.50
JAD 00766
Temporal
lobe structure by magnetic resonance in bipolar affective disorders and schizophrenia *
Alessandro Rossi I, Paolo Stratta ‘, Vittorio Di Michele ‘, Massimo Gallucci Alessandra Splendiani 2, Stefano de Cataldo ’ and Massimo Casacchia ’ Deportments
of ’ Psychiatry and ’ Radiology,
Uniuersity of L’Aquila, I-67100 L’Aquila,
‘,
Itaiy
(Received 12 June 1990) (Revision received 6 September 1990) (Accepted 24 September 1990)
Summary Sixteen bipolar and 10 schizophrenic patients, all male, underwent magnetic resonance imaging scans. Areas derived from five coronal sections were measured separately and then summed to obtain an estimate of temporal lobe volumes. Schizophrenics showed a reduction of temporal lobe areas in those sections corresponding to the hippocampal region. This finding was more pronounced for the left side, although no diagnosis by side interaction was present. Temporal lobe volume was also reduced in schizophrenics. When a lateralized difference was present, the right temporal lobe was larger than the left in both patient groups.
Key words: Bipolar
affective
disorder;
Schizophrenia;
Introduction Several types of structural brain abnormalities have been found in schizophrenia (Shelton and Weinberger, 1986) and more recently positive findings have been reported in affective disorders, especially bipolar ones (Jeste et al., 1988). How-
Address for correspondence: Dr. Alessandro Psichiatrica. Ospedale S. Maria di Collemaggio. L’AquiIa, I-67100 L’Aquila, Italy. * Presented Psychiatric
Rossi, Clinica Universita de
at the 143rd Annual Meeting of the American Association, New York, May 12-17. 1990.
Magnetic
resonance
imaging;
Temporal
lobes
ever, the measurements of gross indexes of brain damage, such as ventricular brain ratio (VBR), sulcal widening or cerebellar atrophy, mainly from computed tomography (CT) reports, have not allowed a clear-cut discrimination between the meaning of the reported abnormalities in the brain of schizophrenics and those of bipolar patients (Jeste et al., 1988). We hypothesize that the study of temporal lobe anatomy may add further clues to the pathophysiological meaning of any brain abnormalities in schizophrenia and bipolar affective disorder. The present magnetic resonance imaging (MRI) study was designed to further explore our hypothesis, evaluating temporal lobe structure in schizophrenia versus bipolar disorder.
20
Method Twenty DSM-III bipolar patients and 15 chronic or subchronic schizophrenic patients, all consecutively admitted, gave informed consent for an MRI procedure. The study was limited to male patients. No patient had history of institutionalization. MR images were made with an Ansaldo Esatom 5000, 0.5 Tesla scanner using an SE sequence (TR 2400, TE 120 ms) to obtain 15 coronal slices (5 mm thick, 2 mm interslice gap) after a midsagittal pilot scan (TR 220, TE 20) was obtained. The coronal plane was oriented perpendicularly to the ethmoidal plane. We decided to measure temporal lobe areas in five slices (usually 5-9 in postero-anterior direction) although the lobe was also clearly visualized in slices 4, 10 and 11. We chose those sections because they were easily anchored to anatomical brain regions (see Anatomical measurements). Slice selection was done according to Daniels et al.‘s (1987) atlas (pp. 50-57). One bipolar and two schizophrenic patients had unusable midsagittal images, three bipolar and three schizophrenic patients had unusable
coronal images due to movement artifacts or incorrect slice position. Eventually usable scans were obtained from 16 bipolars (mean age k SD 47.00 k 11.98 years) and 10 schizophrenics (mean age k SD 28.60 k 5.12 years). There was no significant difference between the schizophrenic and bipolar groups for height (mean + SD 174.9 f 8.9 and 171.7 + 9.9 cm). All subjects were right-handed. Anatomical measurements The structural measurements were performed by a senior neuroradiologist (M.G.) who was unaware of the identity of the subjects. Structures were identified with the help of the cited MRI atlas and all the measures made by a blind scorer. Temporal lobes were defined on slices 9 and 8 usually showing the amygdala, slices 7 and 6 usually showing the hippocampus and slice 5 showing temporal lobes at the coronal plane passing through the posterior body and the splenium of the corpus callosum. On the midsagittal section the cortical area was also measured as described in our earlier study (Rossi et al., 1989). Measurements were done manually from film onto a digitizing tablet (Digitizer KD 3300) interfaced to an
TABLE 1 TEMPORAL Slice
LOBE AREAS AND VOLUMES IN SCHIZOPHRENIC Measure a
Schizophrenics (mean * SD)
(n = 10) AND BIPOLAR (n = 16) PATIENTS
Bipolars (mean + SD)
Twc-way mixed ANOVA Group (A) factor (df=1,23)
Side (B) factor (df=1,24)
AxB interaction (d/=1,24)
5
Right
Temporal lobe areas (cm*) 13.67k3.17
15.39 f 2.46
F= 4.76 +
F=17.33
6
Left Right
12.90 f 2.36 13.39k1.70
14.01* 1.93 14.23 + 2.60
F=8.34
F = 4.45 *
F = 0.14
7
Left Right
12.54+1.84 13.63 + 2.54
13.64+3.04 14.04k1.96
F= 5.38 *
F = 1.92
F = 0.85
8
Left Right
12.95 f 1.49 14.34 k 2.38
13.91 f 2.66 14.98 f 2.55
F = 2.02
F= 5.79 +
F = 2.98
9
Left Right
13.09k 1.18 12.65 k 1.87
14.78 f 2.82 13.29 f 2.25
F = 0.39
F=1.91
F=1.64
Left
11.925 1.60
13.26 f 2.54
Temporgd lobe volumes (cm3) 33.85 i4.96 Left 31.71& 3.37
35.91 f 5.02
Right
34.80 f 5.64
a Measurements are actual areas and volumes. * P < 0.05, * * P < 0.01, * * * P < 0.001, * * * * P i o.ooo5.
F=4.60
**
*
F=13.16
****
***
F=1.37
F=1.13
21
IBM AT equipped with Autocad as previously described (Rossi et al., 1990a). Examining test-retest reliability, the same rater blindly selected 40 temporal area images for repeated measurements at a later date. The two tracings of the temporal lobe size yielded a Pearson correlation coefficient of 0.92. Results Because the two groups differed substantially in age, this variable was covariate. The two-way mixed ANOVA with diagnosis as between-group factor and hemisphere as within-group factor is shown in Table 1. When univariate F ratios between groups with age as covariate were calculated, the right temporal lobe was reduced in schizophrenics slices 5 and 6 (F(1,23) = 4.50, P < 0.05 and F(1,23) = 7.04, P < 0.015respectively) and the left temporal lobe in slices 5, 6, 7 and 8 (F(1,23) = 4.48, P < 0.05; F(1,23) = 7.16, P < 0.015; F(1,23) = 5.35, P -c0.05; and F(1,23) = 4.35, P < 0.05 respectively). When the five area measurements were totalled to obtain a measure of temporal lobe volume, schizophrenics showed a reduced left and right temporal lobe volume and both groups had a larger right than left temporal lobe volume (Table 1). To check for a possible confounding effect of a measure of brain size, the midsagittal cerebral area was also covariated but no significant effect on temporal lobe measurements was observed. Discussion This study has revealed differences in temporal lobe structure between schizophrenic patients and a comparison group of manic depressive patients. Schizophrenics show reduced temporal lobe volumes and, in those slices corresponding to the region containing the hippocampus, reduced temporal lobe areas. Moreover the left side seems to have a major role in this reduction although we were unable to find a side by status interaction in the statistical analysis. Previous studies have shown schizophrenics to have a reduction of the temporal lobe gray matter in the right and left central sections when compared to healthy subjects (Suddath et al., 1989),
but only one study has addressed the issue of possible differences between schizophrenics and bipolars (Johnstone et al., 1989). This study reported a reduction of temporal lobe area with a diagnosis by side interaction, the area being less on the left than the right side, in contrast to findings in bipolar affective disorder and normal controls (Johnstone et al., 1989). For measurement purposes the authors selected, from among six to ten slices, the section with the largest measured area. Interestingly this slice could be approximated to our slice ‘8 and for this slice we found the largest F ratio for diagnosis by side interaction. In other words it seems that going in a postero-anterior direction our bipolar patients and the two non-schizophrenic groups of the Johnstone et al. study have fewer right-left differences than the schizophrenics. In studies similar to our own the mean temporal lobe volumes were 59 cm3 on the right and 51 cm3 on the left (Jack et al., 1988) and 85.6 cm3 on the right and 74.1 cm3 on the left (Suddath et al., 1989) in healthy controls. Differences between these two studies have been previously discussed (Suddath et al., 1989) while differences between our findings (35.97 cm3 on the right and 34.80 cm3 on the left temporal lobe’ in bipolar patients) and those mentioned above are related to our adoption of non-contiguous slice selection with a 2-mm interslice gap and to a temporal lobe measurement limited to the central appearance. In fact we do not use the most posterior (slice 4) and most anterior (slices 10 and 11) slice measurements here. Interestingly we confirm our previous finding on laterality in schizophrenia (Rossi et al., 1990) in that the left temporal lobe was smaller than the right and we show a laterality effect in bipolar patients too. This right-left temporal lobe asymmetry has nonetheless been reported in two independent normative MR studies in young adults (Jack et al., 1988, 1989). In discussing our findings of asymmetry, it is also important to emphasize that the between-group differences in temporal lobe areas were seen to be bilateral, although more marked for the left side of schizophrenics. We did not find evidence of lateralized pathology among schizophrenics, which has been reported by Johnstone et al. (1989). However, we underline that measurement of a single slice might
22
give information otherwise lost if this slice had been included in the volume of larger structures. For example temporal lobe volume asymmetry in healthy volunteers (Jack et al., 1988, 1989; Rossi et al., 1990a) may be ‘dissected’ into different levels of asymmetry ranging from marked asymmetry in more posterior temporal regions to no asymmetry in more anterior regions. The latter observation could account for diagnosis by side interaction in a two-way ANOVA model (Johnstone et al., 1989; Rossi et al., 1990b) when these groups of healthy controls are compared with schizophrenics who maintain a level of right-left asymmetry also in the more anterior temporal lobe region because of a left side atrophy or aplasia. Studies such as this may be useful in detecting a level of cerebral abnormalities between two affected samples even though a healthy control group will be important to detect more severe brain abnormalities. Acknowledgement Supported in part by grants from Consiglio Nazionale delle Ricerche (No. 89.02478.04 and No. 89.00328.75). * References Daniels, D.L., Haughton, V.M. and Naidich, T.P. (1987) Cranial and Spinal Magnetic Resonance Imaging: An Atlas and Guide. Raven Press, New York, NY. Jack, C.R., Gehring, D.G. and Sharbrough, F.W. (1988) Tem-
poral lobe measurement from MR images: accuracy and left-right asymmetry in normal persons. J. Comput. Assist. Tomogr. 12. 21. Jack, C.R., Twomey, C.K., Zinsmeister, A.R., Sharbrough, F.W.. Petersen, R.C. and Cascino, G.D. (1989) Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 172, 549. Jeste, D.V.. Lohr, J.B. and Goodwin, F.K. (1988) Neuroanatomical studies of major affective disorders. A review and suggestions for further research. Br. J. Psychiatry 153, 444. Johnstone, E.C., Cowens, D.G., Crow, T.J.. Frith, CD., Alexandropohs, R., Bydder, G. and Colter. N. (1989) Temporal lobe structure as determined by nuclear magnetic resonance in schizophrenia and bipolar affective disorder. J. Neurol. Neurosurg. Psychiatry 52, 736. Rossi, A., Stratta, P., Gallucci. M.. Passariello, R. and Casacchia, M. (1989) Quantification of corpus callosum and ventricles in schizophrenia with nuclear magnetic resonance imaging: a pilot study. Am. J. Psychiatry 146, 99. Rossi, A., Stratta, P., D’Albenzio, L., Tartaro, A., Schiazza, G., Di Michele, V., Bolino. F. and Casacchia. M. (1990) Reduced temporal lobe areas in schizophrenia. Biol. Psychiatry 27. 61. Rossi, A., Stratta, P., D’Albenzio, L.. Tartaro, A., Schiazza, G., Di Michele. V. and Casacchia, M. (1990b) Temporal lobe structure in schizophrenia: a controlled multiplanar MR study. Biol. Psychiatry 27, 58A. Shelton, R.C. and Weinberger, D.R. (1986) X-ray computerized tomography studies in schizophrenia: a review and synthesis. In: H.A. Nasrallah and D.R. Weinberger (Eds.), The Neurology of Schizophrenia. Elsevier, Amsterdam, pp. 207-250. Suddath. R.L., Casanova, M.F.. Goldberg, T.E., Daniel, D.G., Kelsoe, J.R. and Weinberger. D.R. (1989) Temporal lobe pathology in schizophrenia: a quantitative magnetic resonance imaging study. Am. J. Psychiatry 146, 464.
19 Division)
0165-0327/91/$03.50
JAD 00766
Temporal
lobe structure by magnetic resonance in bipolar affective disorders and schizophrenia *
Alessandro Rossi I, Paolo Stratta ‘, Vittorio Di Michele ‘, Massimo Gallucci Alessandra Splendiani 2, Stefano de Cataldo ’ and Massimo Casacchia ’ Deportments
of ’ Psychiatry and ’ Radiology,
Uniuersity of L’Aquila, I-67100 L’Aquila,
‘,
Itaiy
(Received 12 June 1990) (Revision received 6 September 1990) (Accepted 24 September 1990)
Summary Sixteen bipolar and 10 schizophrenic patients, all male, underwent magnetic resonance imaging scans. Areas derived from five coronal sections were measured separately and then summed to obtain an estimate of temporal lobe volumes. Schizophrenics showed a reduction of temporal lobe areas in those sections corresponding to the hippocampal region. This finding was more pronounced for the left side, although no diagnosis by side interaction was present. Temporal lobe volume was also reduced in schizophrenics. When a lateralized difference was present, the right temporal lobe was larger than the left in both patient groups.
Key words: Bipolar
affective
disorder;
Schizophrenia;
Introduction Several types of structural brain abnormalities have been found in schizophrenia (Shelton and Weinberger, 1986) and more recently positive findings have been reported in affective disorders, especially bipolar ones (Jeste et al., 1988). How-
Address for correspondence: Dr. Alessandro Psichiatrica. Ospedale S. Maria di Collemaggio. L’AquiIa, I-67100 L’Aquila, Italy. * Presented Psychiatric
Rossi, Clinica Universita de
at the 143rd Annual Meeting of the American Association, New York, May 12-17. 1990.
Magnetic
resonance
imaging;
Temporal
lobes
ever, the measurements of gross indexes of brain damage, such as ventricular brain ratio (VBR), sulcal widening or cerebellar atrophy, mainly from computed tomography (CT) reports, have not allowed a clear-cut discrimination between the meaning of the reported abnormalities in the brain of schizophrenics and those of bipolar patients (Jeste et al., 1988). We hypothesize that the study of temporal lobe anatomy may add further clues to the pathophysiological meaning of any brain abnormalities in schizophrenia and bipolar affective disorder. The present magnetic resonance imaging (MRI) study was designed to further explore our hypothesis, evaluating temporal lobe structure in schizophrenia versus bipolar disorder.
20
Method Twenty DSM-III bipolar patients and 15 chronic or subchronic schizophrenic patients, all consecutively admitted, gave informed consent for an MRI procedure. The study was limited to male patients. No patient had history of institutionalization. MR images were made with an Ansaldo Esatom 5000, 0.5 Tesla scanner using an SE sequence (TR 2400, TE 120 ms) to obtain 15 coronal slices (5 mm thick, 2 mm interslice gap) after a midsagittal pilot scan (TR 220, TE 20) was obtained. The coronal plane was oriented perpendicularly to the ethmoidal plane. We decided to measure temporal lobe areas in five slices (usually 5-9 in postero-anterior direction) although the lobe was also clearly visualized in slices 4, 10 and 11. We chose those sections because they were easily anchored to anatomical brain regions (see Anatomical measurements). Slice selection was done according to Daniels et al.‘s (1987) atlas (pp. 50-57). One bipolar and two schizophrenic patients had unusable midsagittal images, three bipolar and three schizophrenic patients had unusable
coronal images due to movement artifacts or incorrect slice position. Eventually usable scans were obtained from 16 bipolars (mean age k SD 47.00 k 11.98 years) and 10 schizophrenics (mean age k SD 28.60 k 5.12 years). There was no significant difference between the schizophrenic and bipolar groups for height (mean + SD 174.9 f 8.9 and 171.7 + 9.9 cm). All subjects were right-handed. Anatomical measurements The structural measurements were performed by a senior neuroradiologist (M.G.) who was unaware of the identity of the subjects. Structures were identified with the help of the cited MRI atlas and all the measures made by a blind scorer. Temporal lobes were defined on slices 9 and 8 usually showing the amygdala, slices 7 and 6 usually showing the hippocampus and slice 5 showing temporal lobes at the coronal plane passing through the posterior body and the splenium of the corpus callosum. On the midsagittal section the cortical area was also measured as described in our earlier study (Rossi et al., 1989). Measurements were done manually from film onto a digitizing tablet (Digitizer KD 3300) interfaced to an
TABLE 1 TEMPORAL Slice
LOBE AREAS AND VOLUMES IN SCHIZOPHRENIC Measure a
Schizophrenics (mean * SD)
(n = 10) AND BIPOLAR (n = 16) PATIENTS
Bipolars (mean + SD)
Twc-way mixed ANOVA Group (A) factor (df=1,23)
Side (B) factor (df=1,24)
AxB interaction (d/=1,24)
5
Right
Temporal lobe areas (cm*) 13.67k3.17
15.39 f 2.46
F= 4.76 +
F=17.33
6
Left Right
12.90 f 2.36 13.39k1.70
14.01* 1.93 14.23 + 2.60
F=8.34
F = 4.45 *
F = 0.14
7
Left Right
12.54+1.84 13.63 + 2.54
13.64+3.04 14.04k1.96
F= 5.38 *
F = 1.92
F = 0.85
8
Left Right
12.95 f 1.49 14.34 k 2.38
13.91 f 2.66 14.98 f 2.55
F = 2.02
F= 5.79 +
F = 2.98
9
Left Right
13.09k 1.18 12.65 k 1.87
14.78 f 2.82 13.29 f 2.25
F = 0.39
F=1.91
F=1.64
Left
11.925 1.60
13.26 f 2.54
Temporgd lobe volumes (cm3) 33.85 i4.96 Left 31.71& 3.37
35.91 f 5.02
Right
34.80 f 5.64
a Measurements are actual areas and volumes. * P < 0.05, * * P < 0.01, * * * P < 0.001, * * * * P i o.ooo5.
F=4.60
**
*
F=13.16
****
***
F=1.37
F=1.13
21
IBM AT equipped with Autocad as previously described (Rossi et al., 1990a). Examining test-retest reliability, the same rater blindly selected 40 temporal area images for repeated measurements at a later date. The two tracings of the temporal lobe size yielded a Pearson correlation coefficient of 0.92. Results Because the two groups differed substantially in age, this variable was covariate. The two-way mixed ANOVA with diagnosis as between-group factor and hemisphere as within-group factor is shown in Table 1. When univariate F ratios between groups with age as covariate were calculated, the right temporal lobe was reduced in schizophrenics slices 5 and 6 (F(1,23) = 4.50, P < 0.05 and F(1,23) = 7.04, P < 0.015respectively) and the left temporal lobe in slices 5, 6, 7 and 8 (F(1,23) = 4.48, P < 0.05; F(1,23) = 7.16, P < 0.015; F(1,23) = 5.35, P -c0.05; and F(1,23) = 4.35, P < 0.05 respectively). When the five area measurements were totalled to obtain a measure of temporal lobe volume, schizophrenics showed a reduced left and right temporal lobe volume and both groups had a larger right than left temporal lobe volume (Table 1). To check for a possible confounding effect of a measure of brain size, the midsagittal cerebral area was also covariated but no significant effect on temporal lobe measurements was observed. Discussion This study has revealed differences in temporal lobe structure between schizophrenic patients and a comparison group of manic depressive patients. Schizophrenics show reduced temporal lobe volumes and, in those slices corresponding to the region containing the hippocampus, reduced temporal lobe areas. Moreover the left side seems to have a major role in this reduction although we were unable to find a side by status interaction in the statistical analysis. Previous studies have shown schizophrenics to have a reduction of the temporal lobe gray matter in the right and left central sections when compared to healthy subjects (Suddath et al., 1989),
but only one study has addressed the issue of possible differences between schizophrenics and bipolars (Johnstone et al., 1989). This study reported a reduction of temporal lobe area with a diagnosis by side interaction, the area being less on the left than the right side, in contrast to findings in bipolar affective disorder and normal controls (Johnstone et al., 1989). For measurement purposes the authors selected, from among six to ten slices, the section with the largest measured area. Interestingly this slice could be approximated to our slice ‘8 and for this slice we found the largest F ratio for diagnosis by side interaction. In other words it seems that going in a postero-anterior direction our bipolar patients and the two non-schizophrenic groups of the Johnstone et al. study have fewer right-left differences than the schizophrenics. In studies similar to our own the mean temporal lobe volumes were 59 cm3 on the right and 51 cm3 on the left (Jack et al., 1988) and 85.6 cm3 on the right and 74.1 cm3 on the left (Suddath et al., 1989) in healthy controls. Differences between these two studies have been previously discussed (Suddath et al., 1989) while differences between our findings (35.97 cm3 on the right and 34.80 cm3 on the left temporal lobe’ in bipolar patients) and those mentioned above are related to our adoption of non-contiguous slice selection with a 2-mm interslice gap and to a temporal lobe measurement limited to the central appearance. In fact we do not use the most posterior (slice 4) and most anterior (slices 10 and 11) slice measurements here. Interestingly we confirm our previous finding on laterality in schizophrenia (Rossi et al., 1990) in that the left temporal lobe was smaller than the right and we show a laterality effect in bipolar patients too. This right-left temporal lobe asymmetry has nonetheless been reported in two independent normative MR studies in young adults (Jack et al., 1988, 1989). In discussing our findings of asymmetry, it is also important to emphasize that the between-group differences in temporal lobe areas were seen to be bilateral, although more marked for the left side of schizophrenics. We did not find evidence of lateralized pathology among schizophrenics, which has been reported by Johnstone et al. (1989). However, we underline that measurement of a single slice might
22
give information otherwise lost if this slice had been included in the volume of larger structures. For example temporal lobe volume asymmetry in healthy volunteers (Jack et al., 1988, 1989; Rossi et al., 1990a) may be ‘dissected’ into different levels of asymmetry ranging from marked asymmetry in more posterior temporal regions to no asymmetry in more anterior regions. The latter observation could account for diagnosis by side interaction in a two-way ANOVA model (Johnstone et al., 1989; Rossi et al., 1990b) when these groups of healthy controls are compared with schizophrenics who maintain a level of right-left asymmetry also in the more anterior temporal lobe region because of a left side atrophy or aplasia. Studies such as this may be useful in detecting a level of cerebral abnormalities between two affected samples even though a healthy control group will be important to detect more severe brain abnormalities. Acknowledgement Supported in part by grants from Consiglio Nazionale delle Ricerche (No. 89.02478.04 and No. 89.00328.75). * References Daniels, D.L., Haughton, V.M. and Naidich, T.P. (1987) Cranial and Spinal Magnetic Resonance Imaging: An Atlas and Guide. Raven Press, New York, NY. Jack, C.R., Gehring, D.G. and Sharbrough, F.W. (1988) Tem-
poral lobe measurement from MR images: accuracy and left-right asymmetry in normal persons. J. Comput. Assist. Tomogr. 12. 21. Jack, C.R., Twomey, C.K., Zinsmeister, A.R., Sharbrough, F.W.. Petersen, R.C. and Cascino, G.D. (1989) Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 172, 549. Jeste, D.V.. Lohr, J.B. and Goodwin, F.K. (1988) Neuroanatomical studies of major affective disorders. A review and suggestions for further research. Br. J. Psychiatry 153, 444. Johnstone, E.C., Cowens, D.G., Crow, T.J.. Frith, CD., Alexandropohs, R., Bydder, G. and Colter. N. (1989) Temporal lobe structure as determined by nuclear magnetic resonance in schizophrenia and bipolar affective disorder. J. Neurol. Neurosurg. Psychiatry 52, 736. Rossi, A., Stratta, P., Gallucci. M.. Passariello, R. and Casacchia, M. (1989) Quantification of corpus callosum and ventricles in schizophrenia with nuclear magnetic resonance imaging: a pilot study. Am. J. Psychiatry 146, 99. Rossi, A., Stratta, P., D’Albenzio, L., Tartaro, A., Schiazza, G., Di Michele, V., Bolino. F. and Casacchia. M. (1990) Reduced temporal lobe areas in schizophrenia. Biol. Psychiatry 27. 61. Rossi, A., Stratta, P., D’Albenzio, L.. Tartaro, A., Schiazza, G., Di Michele. V. and Casacchia, M. (1990b) Temporal lobe structure in schizophrenia: a controlled multiplanar MR study. Biol. Psychiatry 27, 58A. Shelton, R.C. and Weinberger, D.R. (1986) X-ray computerized tomography studies in schizophrenia: a review and synthesis. In: H.A. Nasrallah and D.R. Weinberger (Eds.), The Neurology of Schizophrenia. Elsevier, Amsterdam, pp. 207-250. Suddath. R.L., Casanova, M.F.. Goldberg, T.E., Daniel, D.G., Kelsoe, J.R. and Weinberger. D.R. (1989) Temporal lobe pathology in schizophrenia: a quantitative magnetic resonance imaging study. Am. J. Psychiatry 146, 464.
