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December 1995, Vol 52, No. 12 >
Article | December 1995

Frontal and Temporal Lobe Brain Volumes in Schizophrenia: Title and subTitle BreakRelationship to Symptoms and Clinical Subtype

Bruce Turetsky, MD; Patricia E. Cowell, PhD; Ruben C. Gur, PhD; Robert I. Grossman, MD; Derri L. Shtasel, MD; Raquel E. Gur, MD, PhD
Arch Gen Psychiatry. 1995;52(12):1061-1070. doi:10.1001/archpsyc.1995.03950240079013
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Background:  Quantitative magnetic resonance imaging (MRI) studies demonstrate reduced brain volumes in schizophrenics, but specific structural abnormalities have not been clearly delineated. The structural abnormalities of this disorder are likely to be heterogeneous, consistent with its diverse clinical presentation. To investigate the relationship between structural abnormality and clinical symptoms, we examined regional brain and cerebral spinal fluid (CSF) volumes in a large sample of schizophrenic patients and controls, with patients aggregated into clinical subtypes.

Methods:  Right and left hemisphere frontal and temporal lobe brain and CSF volumes were quantified from 5-mm axial spin-echo MRIs for 71 schizophrenic patients and 77 age- and sex-matched controls. The following four standardized rating scales were used to assess symptom severity: Negative Symptoms, Disorganization, Schneiderian Delusions and Hallucinations, and Suspicion-Hostility. Patients were also subtyped as either deficit or nondeficit on the basis of enduring negative symptoms.

Results:  Schizophrenic patients overall exhibited ab-a normal brain asymmetry, with selective decrease in brain volume in the left temporal and right frontal regions. Left temporal lobe parenchymal volume reduction and CSF volume increase were correlated with the severity of negative symptoms. Consistent with this, the subtype analysis revealed abnormal temporal lobe asymmetry for the deficit subgroup only. Right frontal lobe volume reduction correlated with the duration of illness, independent of symptom severity or schizophrenic subtype.

Conclusions:  Abnormal lateral asymmetry suggests selective structural deficits in schizophrenia, rather than diffusely undifferentiated CNS abnormalities. The pattern of regional abnormalities is related to clinical symptoms, with negative symptoms being associated with left temporal lobe rather than frontal lobe abnormality. This is consistent with suggestions of a temporolimbic prefrontal network abnormality in schizophrenia. Further longitudinal studies are warranted, using higherresolution MRI technology and gray matter—white matter segmentation to confirm and extend these findings.

REFERENCES

1 +
Pfefferbaum A, Zipursky RB, Lim KO, Zatz LM, Stahl SM, Jernigan TL.  Computed tomographic evidence for generalized sulcal and ventricular enlargement in schizophrenia . Arch Gen Psychiatry . 1988;;45:633-640.
2 +
Gur RE, Mozley PD, Resnick SM, Shtasel D, Kohn M, Zimmerman R, Herman G, Atlas S, Grossman R, Erwin R, Gur RC.  Magnetic resonance imaging in schizophrenia, I: volumetric analysis of brain and cerebrospinal fluid . Arch Gen Psychiatry . 1991;;48:407-412.
3 +
Pearlson GD, Kim WS, Kubos KL, Moberg PJ, Jayaram G, Bascom MJ, Chase GA, Goldfinger AD, Tune LE.  Ventricle-brain ratio, computed tomographic density, and brain area in 50 schizophrenics . Arch Gen Psychiatry . 1989;;46:690-697.
4 +
Kelsoe JR, Cadet JL, Pickar D, Weinberger DR.  Quantitative neuroanatomy in schizophrenia: a controlled magnetic resonance imaging study . Arch Gen Psychiatry . 1988;;45:533-541.
5 +
Andreasen NC, Nasrallah HA, Dunn V, Olson SC, Grove WM, Ehrhardt JC, Coffman JA, Crossett JHW.  Structural abnormalities in the frontal system in schizophrenia: a magnetic resonance imaging study . Arch Gen Psychiatry . 1986;;43:136-144.
6 +
Dauphinais D, DeLisi LE, Crow TJ, Alexandropoulos K, Colter N, Tuma I, Gershon ES.  Reduction in temporal lobe size in siblings with schizophrenia: a magnetic resonance imaging study . Psychiatry Res Neuroimaging . 1990;;35:137-147.
7 +
Suddath RL, Casanova MF, Goldberg TE, Daniel DG, Kelsoe JR, Weinberger DR.  Temporal lobe pathology in schizophrenia . Am J Psychiatry . 1989;;1146:464-472.
8 +
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;;322:789-794.
9 +
Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE.  Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia . Am J Psychiatry . 1990;;147:1457-1462.
10 +
Bogerts B, Ashtari M, Degreet G, Alvir JM, Bilder RM, Lieberman JA.  Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia . Psychiatry Res Neuroimaging . 1990;;35:1-13.
11 +
Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, Hokama H, Martin J, Metcalf D, Coleman M, McCarley RW.  Abnormalities of the left temporal lobe and thought disorder in schizophrenia: a quantitative magnetic resonance imaging study . N Engl J Med . 1992;;327:604-612.
12 +
DeLisi LE, Hoff AL, Schwartz JE, Shields GW, Halthore SN, Gupta SM, Henn FA, Anand AK.  Brain morphology in first-episode schizophrenic-like psychotic patients: a quantitative magnetic resonance imaging study . Biol Psychiatry . 1991;;29:159-175.
13 +
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.
14 +
Mozley PD, Gur RE, Resnick SM, Shtasel DL, Richards J, Kohn M, Grossman R, Herman G, Gur RC.  Magnetic resonance imaging in schizophrenia: relationship with clinical measures . Schizophr Res . 1994;;12:195-203.
15 +
Gur RE, Mozley PD, Shtasel DL, Cannon TD, Gallacher F, Turetsky B, Grossman R, Gur RC.  Clinical subtypes of schizophrenia: differences in brain and CSF volume . Am J Psychiatry . 1994;;151:343-350.
16 +
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Revised Third Edition . Washington, DC: American Psychiatric Association; 1987;.
17 +
Spitzer RL, Williams JBW, Gibbon M. Structured Clinical Interview for DSM-III-R—Patient Version (SCID-P) . New York, NY: New York State Psychiatric Institute; 1986;.
18 +
Shtasel DL, Gur RE, Gallacher F, Heimberg C, Cannon TD, Gur RC.  Phenomenology and functioning in first-episode schizophrenia . Schizophr Bull . 1992;;18:449-462.
19 +
Gur RE.  Motoric laterality imbalance in schizophrenia: a possible concomitant of left hemisphere dysfunction . Arch Gen Psychiatry . 1977;;34:33-37.
20 +
Spitzer RL, Williams JBW, Gibbon M. Structured Clinical Interview for DSM-III-R—Nonpatient Version (SCID-NP) . New York, NY: New York State Psychiatric Institute; 1987;.
21 +
Shtasel DL, Gur RE, Mozley PD, Richards J, Taleff MM, Heimberg C, Gallacher F, Gur RC.  Volunteers for biomedical research: recruitment and screening of normal controls . Arch Gen Psychiatry . 1991;;48:1022-1025.
22 +
Overall JR, Gorham DR.  The Brief Psychiatric Rating Scale . J Operat Psychiatry . 1980;;11:48-64.
23 +
Andreasen NC. The Scale for the Assessment of Negative Symptoms (SANS) . Iowa City, Iowa: The University of Iowa; 1983;.
24 +
Andreasen NC. The Scale for the Assessment of Positive Symptoms (SAPS) . Iowa City, Iowa: The University of Iowa; 1984;.
25 +
Strauss JS, Carpenter WT.  Characteristic symptoms and outcome in schizophrenia . Arch Gen Psychiatry . 1974;;30:429-434.
26 +
Liddle PF.  The symptoms of chronic schizophrenia: a re-examination of the positive-negative dichotomy . Br J Psychiatry . 1987;;151:145-151.
27 +
Arndt S, Alliger RJ, Andreasen NC.  The positive and negative distinction: failure of the two-dimensional model . Br J Psychiatry . 1991;;158:317-322.
28 +
Cronbach LJ.  Coefficient alpha and the internal structure of tests . Psychometrika . 1951;;16:297-234.
29 +
Hase HD, Goldberg LR.  Comparative validity of different strategies of constructing personality inventory scales . Psychol Bull . 1967;;67:231-248.
30 +
Carpenter WT, Heinrichs DW, Wagman AMI.  Deficit and nondeficit forms of schizophrenia: the concept . Am J Psychiatry . 1988;;145:578-583.
31 +
Cowell PE, Turetsky B, Gur RC, Grossman RI, Shtasel DL, Gur RE.  Sex differences in aging of the human frontal and temporal lobes . J Neurosci . 1994;;14:4748-4755.
32 +
Kohn MI, Tanna NK, Herman GT, Resnick SM, Mozley PD, Gur RE, Alavi A, Zimmerman RA, Gur RC.  Analysis of brain and CSF volumes from magnetic resonance imaging: methodology, reliability and validation . Radiology . 1991;;178:115-122.
33 +
Saykin AJ, Gur RC, Gur RE, Mozley DP, Mozley LH, Resnick SM, Kester DB, Stafiniak P.  Neuropsychological function in schizophrenia: selective impairment in memory and learning . Arch Gen Psychiatry . 1991;;48:618-624.
34 +
Bogerts B.  Recent advances in the neuropathology of schizophrenia . Schizophr Bull . 1993;;19:431-445.
35 +
Fuster JM. The Prefrontal Cortex . New York, NY: Raven Press; 1989;.
36 +
Andreasen NC, Rezai K, Alliger R, Swayze VW, Flaum P, Kirchner P, Cohen G, O'Leary DS.  Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia: assessment with xenon 133 single-photon emission computed tomography and the Tower of London . Arch Gen Psychiatry . 1992;;49:943-958.
37 +
Liddle PF, Friston KJ, Frith CD, Hirsch SR, Jones T, Frackowiak RSJ.  Patterns of cerebral blood flow in schizophrenia . Br J Psychiatry . 1992;;60:179-186.
38 +
Andreasen NC, Nasrallah HA, Dunn V, Olson SC, Grove WM, Ehrhardt JC, Coffman JA, Crossett JHW.  Structural abnormalities in the frontal system in schizophrenia: a magnetic resonance imaging study . Arch Gen Psychiatry . 1986;;43:136-144.
39 +
Andreasen NC, Ehrhardt JC, Swayze VW, Alliger RJ, Yuh WTC, Cohen G, Ziebell S.  Magnetic resonance imaging of the brain in schizophrenia: the pathophysiologic significance of structural abnormalities . Arch Gen Psychiatry . 1990;;47:35-44.
40 +
Jackson JH.  On the anatomical and physiological localization of movements in the brain . Lancet . 1873;;1:84-85, 162-164, 232-234.
41 +
Lipska BK, Weinberger DR.  Delayed effects of neonatal hippocampal damage on haloperidol-induced catalepsy and apomorphine-induced stereotypic behaviors in the rat . Dev Brain Res . 1993;;75:213-222.
42 +
Lipska BK, Jaskiw GE, Weinberger DR.  Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia . Neuropsychopharmacology . 1993;;9:67-75.
43 +
Kalsbeek A, Voorn P, Buijs RM, Pool CW, Vylings HBM.  Development of the dopaminergic innervation in the prefrontal cortex of the rat . J Comp Neurol . 1988;;269:56-72.
44 +
Weinberger DR, Berman KF, Suddath R, 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;;149:890-897.
45 +
Gur RE, Mozley PD, Resnick SL, Mozley LH, Shtasel DL, Gallacher F, Arnold SE, Karp JS, Alavi A, Reivich M, Gur RC.  Resting cerebral glucose metabolism in first-episode and previously treated patients with schizophrenia relates to clinical features . Arch Gen Psychiatry . 1995;;52:657-667.

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1 +
Pfefferbaum A, Zipursky RB, Lim KO, Zatz LM, Stahl SM, Jernigan TL.  Computed tomographic evidence for generalized sulcal and ventricular enlargement in schizophrenia . Arch Gen Psychiatry . 1988;;45:633-640.
2 +
Gur RE, Mozley PD, Resnick SM, Shtasel D, Kohn M, Zimmerman R, Herman G, Atlas S, Grossman R, Erwin R, Gur RC.  Magnetic resonance imaging in schizophrenia, I: volumetric analysis of brain and cerebrospinal fluid . Arch Gen Psychiatry . 1991;;48:407-412.
3 +
Pearlson GD, Kim WS, Kubos KL, Moberg PJ, Jayaram G, Bascom MJ, Chase GA, Goldfinger AD, Tune LE.  Ventricle-brain ratio, computed tomographic density, and brain area in 50 schizophrenics . Arch Gen Psychiatry . 1989;;46:690-697.
4 +
Kelsoe JR, Cadet JL, Pickar D, Weinberger DR.  Quantitative neuroanatomy in schizophrenia: a controlled magnetic resonance imaging study . Arch Gen Psychiatry . 1988;;45:533-541.
5 +
Andreasen NC, Nasrallah HA, Dunn V, Olson SC, Grove WM, Ehrhardt JC, Coffman JA, Crossett JHW.  Structural abnormalities in the frontal system in schizophrenia: a magnetic resonance imaging study . Arch Gen Psychiatry . 1986;;43:136-144.
6 +
Dauphinais D, DeLisi LE, Crow TJ, Alexandropoulos K, Colter N, Tuma I, Gershon ES.  Reduction in temporal lobe size in siblings with schizophrenia: a magnetic resonance imaging study . Psychiatry Res Neuroimaging . 1990;;35:137-147.
7 +
Suddath RL, Casanova MF, Goldberg TE, Daniel DG, Kelsoe JR, Weinberger DR.  Temporal lobe pathology in schizophrenia . Am J Psychiatry . 1989;;1146:464-472.
8 +
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;;322:789-794.
9 +
Barta PE, Pearlson GD, Powers RE, Richards SS, Tune LE.  Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia . Am J Psychiatry . 1990;;147:1457-1462.
10 +
Bogerts B, Ashtari M, Degreet G, Alvir JM, Bilder RM, Lieberman JA.  Reduced temporal limbic structure volumes on magnetic resonance images in first episode schizophrenia . Psychiatry Res Neuroimaging . 1990;;35:1-13.
11 +
Shenton ME, Kikinis R, Jolesz FA, Pollak SD, LeMay M, Wible CG, Hokama H, Martin J, Metcalf D, Coleman M, McCarley RW.  Abnormalities of the left temporal lobe and thought disorder in schizophrenia: a quantitative magnetic resonance imaging study . N Engl J Med . 1992;;327:604-612.
12 +
DeLisi LE, Hoff AL, Schwartz JE, Shields GW, Halthore SN, Gupta SM, Henn FA, Anand AK.  Brain morphology in first-episode schizophrenic-like psychotic patients: a quantitative magnetic resonance imaging study . Biol Psychiatry . 1991;;29:159-175.
13 +
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.
14 +
Mozley PD, Gur RE, Resnick SM, Shtasel DL, Richards J, Kohn M, Grossman R, Herman G, Gur RC.  Magnetic resonance imaging in schizophrenia: relationship with clinical measures . Schizophr Res . 1994;;12:195-203.
15 +
Gur RE, Mozley PD, Shtasel DL, Cannon TD, Gallacher F, Turetsky B, Grossman R, Gur RC.  Clinical subtypes of schizophrenia: differences in brain and CSF volume . Am J Psychiatry . 1994;;151:343-350.
16 +
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, Revised Third Edition . Washington, DC: American Psychiatric Association; 1987;.
17 +
Spitzer RL, Williams JBW, Gibbon M. Structured Clinical Interview for DSM-III-R—Patient Version (SCID-P) . New York, NY: New York State Psychiatric Institute; 1986;.
18 +
Shtasel DL, Gur RE, Gallacher F, Heimberg C, Cannon TD, Gur RC.  Phenomenology and functioning in first-episode schizophrenia . Schizophr Bull . 1992;;18:449-462.
19 +
Gur RE.  Motoric laterality imbalance in schizophrenia: a possible concomitant of left hemisphere dysfunction . Arch Gen Psychiatry . 1977;;34:33-37.
20 +
Spitzer RL, Williams JBW, Gibbon M. Structured Clinical Interview for DSM-III-R—Nonpatient Version (SCID-NP) . New York, NY: New York State Psychiatric Institute; 1987;.
21 +
Shtasel DL, Gur RE, Mozley PD, Richards J, Taleff MM, Heimberg C, Gallacher F, Gur RC.  Volunteers for biomedical research: recruitment and screening of normal controls . Arch Gen Psychiatry . 1991;;48:1022-1025.
22 +
Overall JR, Gorham DR.  The Brief Psychiatric Rating Scale . J Operat Psychiatry . 1980;;11:48-64.
23 +
Andreasen NC. The Scale for the Assessment of Negative Symptoms (SANS) . Iowa City, Iowa: The University of Iowa; 1983;.
24 +
Andreasen NC. The Scale for the Assessment of Positive Symptoms (SAPS) . Iowa City, Iowa: The University of Iowa; 1984;.
25 +
Strauss JS, Carpenter WT.  Characteristic symptoms and outcome in schizophrenia . Arch Gen Psychiatry . 1974;;30:429-434.
26 +
Liddle PF.  The symptoms of chronic schizophrenia: a re-examination of the positive-negative dichotomy . Br J Psychiatry . 1987;;151:145-151.
27 +
Arndt S, Alliger RJ, Andreasen NC.  The positive and negative distinction: failure of the two-dimensional model . Br J Psychiatry . 1991;;158:317-322.
28 +
Cronbach LJ.  Coefficient alpha and the internal structure of tests . Psychometrika . 1951;;16:297-234.
29 +
Hase HD, Goldberg LR.  Comparative validity of different strategies of constructing personality inventory scales . Psychol Bull . 1967;;67:231-248.
30 +
Carpenter WT, Heinrichs DW, Wagman AMI.  Deficit and nondeficit forms of schizophrenia: the concept . Am J Psychiatry . 1988;;145:578-583.
31 +
Cowell PE, Turetsky B, Gur RC, Grossman RI, Shtasel DL, Gur RE.  Sex differences in aging of the human frontal and temporal lobes . J Neurosci . 1994;;14:4748-4755.
32 +
Kohn MI, Tanna NK, Herman GT, Resnick SM, Mozley PD, Gur RE, Alavi A, Zimmerman RA, Gur RC.  Analysis of brain and CSF volumes from magnetic resonance imaging: methodology, reliability and validation . Radiology . 1991;;178:115-122.
33 +
Saykin AJ, Gur RC, Gur RE, Mozley DP, Mozley LH, Resnick SM, Kester DB, Stafiniak P.  Neuropsychological function in schizophrenia: selective impairment in memory and learning . Arch Gen Psychiatry . 1991;;48:618-624.
34 +
Bogerts B.  Recent advances in the neuropathology of schizophrenia . Schizophr Bull . 1993;;19:431-445.
35 +
Fuster JM. The Prefrontal Cortex . New York, NY: Raven Press; 1989;.
36 +
Andreasen NC, Rezai K, Alliger R, Swayze VW, Flaum P, Kirchner P, Cohen G, O'Leary DS.  Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia: assessment with xenon 133 single-photon emission computed tomography and the Tower of London . Arch Gen Psychiatry . 1992;;49:943-958.
37 +
Liddle PF, Friston KJ, Frith CD, Hirsch SR, Jones T, Frackowiak RSJ.  Patterns of cerebral blood flow in schizophrenia . Br J Psychiatry . 1992;;60:179-186.
38 +
Andreasen NC, Nasrallah HA, Dunn V, Olson SC, Grove WM, Ehrhardt JC, Coffman JA, Crossett JHW.  Structural abnormalities in the frontal system in schizophrenia: a magnetic resonance imaging study . Arch Gen Psychiatry . 1986;;43:136-144.
39 +
Andreasen NC, Ehrhardt JC, Swayze VW, Alliger RJ, Yuh WTC, Cohen G, Ziebell S.  Magnetic resonance imaging of the brain in schizophrenia: the pathophysiologic significance of structural abnormalities . Arch Gen Psychiatry . 1990;;47:35-44.
40 +
Jackson JH.  On the anatomical and physiological localization of movements in the brain . Lancet . 1873;;1:84-85, 162-164, 232-234.
41 +
Lipska BK, Weinberger DR.  Delayed effects of neonatal hippocampal damage on haloperidol-induced catalepsy and apomorphine-induced stereotypic behaviors in the rat . Dev Brain Res . 1993;;75:213-222.
42 +
Lipska BK, Jaskiw GE, Weinberger DR.  Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: a potential animal model of schizophrenia . Neuropsychopharmacology . 1993;;9:67-75.
43 +
Kalsbeek A, Voorn P, Buijs RM, Pool CW, Vylings HBM.  Development of the dopaminergic innervation in the prefrontal cortex of the rat . J Comp Neurol . 1988;;269:56-72.
44 +
Weinberger DR, Berman KF, Suddath R, 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;;149:890-897.
45 +
Gur RE, Mozley PD, Resnick SL, Mozley LH, Shtasel DL, Gallacher F, Arnold SE, Karp JS, Alavi A, Reivich M, Gur RC.  Resting cerebral glucose metabolism in first-episode and previously treated patients with schizophrenia relates to clinical features . Arch Gen Psychiatry . 1995;;52:657-667.

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