TECHNICAL COMMENTARY NeuRA Basal ganglia March 2017 Margarete Ainsworth Building, Barker Street, Randwick NSW 2031. Phone: 02 9399 1000. Email: [email protected]To donate, phone 1800 888 019 or visit www.neura.edu.au/donate/schizophrenia Page 1 Basal ganglia Introduction The basal ganglia are a group of sub-cortical nuclei thought to be involved in motor control and learning. The nuclei comprising the basal ganglia include the caudate, putamen, globus pallidus, the subthalamic nucleus and the substantia nigra. The caudate and putamen together form the striatum, while the globus pallidus (including the ventral pallidum) and the putamen together form the lenticular nucleus. The striatum is the principal input centre, receiving afferents primarily from the cortex, but also the substantia nigra, thalamus, and external globus pallidus. There are two primary pathways from the striatum through the basal ganglia (‘direct’ and ‘indirect’ pathways) which incorporate different components of the basal ganglia circuitry, and play different roles in controlling and planning movements and cognition. Schizophrenia has been associated with altered structure and function of the basal ganglia. Understanding of brain alterations in people with schizophrenia may provide insight into changes in brain development associated with illness onset or progression. Reviews contained in this technical summary reflect structural imaging investigations (MRI), functional imaging investigations (fMRI, PET, SPECT) as well as metabolic imaging (MRS) of basal ganglia function in schizophrenia. Method We have included only systematic reviews (systematic literature search, detailed methodology with inclusion/exclusion criteria) published in full text, in English, from the year 2000 that report results separately for people with a diagnosis of schizophrenia, schizoaffective disorder, schizophreniform disorder or first episode schizophrenia. Reviews were identified by searching the databases MEDLINE, EMBASE, CINAHL, Current Contents, PsycINFO and the Cochrane library. Hand searching reference lists of identified reviews was also conducted. When multiple copies of reviews were found, only the most recent version was included. Reviews with pooled data are prioritised for inclusion. Review reporting assessment was guided by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist, which describes a preferred way to present a meta-analysis 1 . Reviews rated as having less than 50% of items checked have been excluded from the library. The PRISMA flow diagram is a suggested way of providing information about studies included and excluded with reasons for exclusion. Where no flow diagram has been presented by individual reviews, but identified studies have been described in the text, reviews have been checked for this item. Note that early reviews may have been guided by less stringent reporting checklists than the PRISMA, and that some reviews may have been limited by journal guidelines. Evidence was graded using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) Working Group approach where high quality evidence such as that gained from randomised controlled trials (RCTs) may be downgraded to moderate or low if review and study quality is limited, if there is inconsistency in results, indirect comparisons, imprecise or sparse data and high probability of reporting bias. It may also be downgraded if risks associated with the intervention or other matter under review are high. Conversely, low quality evidence such as that gained from observational studies may be upgraded if effect sizes are large, there is a dose dependent response or if results are reasonably consistent, precise and direct with low associated risks (see end of table for an explanation of these terms) 2 . The resulting table represents an objective summary of the available evidence, although the conclusions
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Basal ganglia
Introduction
The basal ganglia are a group of sub-cortical nuclei thought to be involved in motor control and learning. The nuclei comprising the basal ganglia include the caudate, putamen, globus pallidus, the subthalamic nucleus and the substantia nigra. The caudate and putamen together form the striatum, while the globus pallidus (including the ventral pallidum) and the putamen together form the lenticular nucleus.
The striatum is the principal input centre, receiving afferents primarily from the cortex, but also the substantia nigra, thalamus, and external globus pallidus. There are two primary pathways from the striatum through the basal ganglia (‘direct’ and ‘indirect’ pathways) which incorporate different components of the basal ganglia circuitry, and play different roles in controlling and planning movements and cognition.
Schizophrenia has been associated with altered
structure and function of the basal ganglia.
Understanding of brain alterations in people
with schizophrenia may provide insight into
changes in brain development associated with
illness onset or progression. Reviews contained
in this technical summary reflect structural
imaging investigations (MRI), functional
imaging investigations (fMRI, PET, SPECT) as
well as metabolic imaging (MRS) of basal
ganglia function in schizophrenia.
Method
We have included only systematic reviews
(systematic literature search, detailed
methodology with inclusion/exclusion criteria)
published in full text, in English, from the year
2000 that report results separately for people
with a diagnosis of schizophrenia,
schizoaffective disorder, schizophreniform
disorder or first episode schizophrenia.
Reviews were identified by searching the
databases MEDLINE, EMBASE, CINAHL,
Current Contents, PsycINFO and the Cochrane
library. Hand searching reference lists of
identified reviews was also conducted. When
multiple copies of reviews were found, only the
most recent version was included. Reviews with
pooled data are prioritised for inclusion.
Review reporting assessment was guided by
the Preferred Reporting Items for Systematic
Reviews and Meta-Analyses (PRISMA)
checklist, which describes a preferred way to
present a meta-analysis1. Reviews rated as
having less than 50% of items checked have
been excluded from the library. The PRISMA
flow diagram is a suggested way of providing
information about studies included and
excluded with reasons for exclusion. Where no
flow diagram has been presented by individual
reviews, but identified studies have been
described in the text, reviews have been
checked for this item. Note that early reviews
may have been guided by less stringent
reporting checklists than the PRISMA, and that
some reviews may have been limited by journal
guidelines.
Evidence was graded using the Grading of
Recommendations Assessment, Development
and Evaluation (GRADE) Working Group
approach where high quality evidence such as
that gained from randomised controlled trials
(RCTs) may be downgraded to moderate or low
if review and study quality is limited, if there is
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Page 3
Basal ganglia
Chan RCK, Di X, McAlonan GM, Gong Q
Brain Anatomical Abnormalities in High-Risk Individuals, First-Episode, andChronic Schizophrenia: An Activation Likelihood Estimation Meta-analysis of IllnessProgression
Schizophrenia Bulletin 2011; 37(1) 177-188
View review abstract online
Comparison Grey matter volume in people with first episode schizophrenia
vs. healthy controls.
Summary of evidence Moderate quality evidence (large sample size, direct, unable to assess consistency or precision) suggests people with first episode schizophrenia have grey matter reductions in the right caudate nucleus compared to healthy controls, and compared to high risk individuals.
Basal ganglia volume
Meta-analysis was performed using Anatomical Likelihood Estimate (ALE) analysis on Voxel-Based Morphometry MRI studies.
FWHM 10mm, FDR corrected at p < 0.01
14 studies, N = 1082
Right caudate: Talairach coordinates (10, 10, 12), cluster 224mm3, ALE 0.0116
Between group comparisons: subtraction analysis between high risk individuals and first episode schizophrenia
Greater grey matter reduction in first episode group;
Right caudate: Talairach coordinates (10, 8, 14), cluster 224mm3, ALE 0.0104
Left caudate: Talairach coordinates (-12, 6, 12), cluster 192mm3, ALE 0.0099
Consistency in results‡ No measure of consistency is reported.
Precision in results§ No confidence intervals are provided.
Directness of results║ Direct
Ellison-Wright I, Glahn DC, Laird AR, Thelen SM, Bullmore E
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Page 4
Basal ganglia
The anatomy of first-episode and chronic schizophrenia: an anatomical likelihood estimation meta-analysis
American Journal of Psychiatry, 2008. 165(8): 1015-23
View review abstract online
Comparison Grey matter volume in first episode schizophrenia vs. chronic schizophrenia vs. healthy controls.
Summary of evidence Moderate quality evidence (large sample size, direct, unable to assess consistency or precision) suggests reductions in bilateral caudate head grey matter, which are absent in chronic schizophrenia. Increased grey matter was reported in the putamen.
Basal ganglia volume
N = 1556, 27 studies
First episode reductions
Left caudate head: Talairach coordinates (-12, 6, 12), cluster 528mm3, ALE 0.01, p = 0.0002
Right caudate head: Talairach coordinates (10, 10, 12), cluster 1392mm3, ALE 0.012, p < 0.0002
First episode increases
Left putamen: Talairach coordinates (-22, 0, 12), cluster 1592mm3, ALE 0.008, p < 0.0002
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Ellison-Wright I, Bullmore E
Anatomy of bipolar disorder and schizophrenia: A meta-analysis.
Schizophrenia Research 2010; 117: 1-12
View review abstract online
Comparison Grey matter volume in people with schizophrenia vs. healthy
Comparison Functional activation in individuals at high risk of developing schizophrenia vs. healthy controls.
Summary of evidence Low quality evidence (one small observational study per outcome) is unclear as to the direction of the changes in functional activity in the striatum during cognitive tasks in individuals at high risk of developing schizophrenia.
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Page 6
Basal ganglia
Basal ganglia functional activation
1 observational study, N = 32
Large effect size suggests reduced activation of striatum (d = 1.34) in non-psychotic relatives of schizophrenia patients compared to controls for working memory guided saccades.
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Glahn DC, Laird AR, Ellison-Wright I, Thelen SM, Robinson JL, Lancaster JL, Bullmore E, Fox PT
Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis
Biological Psychiatry 2008; 64(9):774-781
View review abstract online
Comparison Grey matter density in people with schizophrenia vs. healthy controls.
Summary of evidence Moderate quality evidence (large sample sizes, direct, unable to assess consistency or precision) suggests schizophrenia is associated with significant increases in grey matter density in the putamen and caudate head in people with schizophrenia.
Basal ganglia volume
Meta-analysis was performed using ALE analysis on Voxel-Based Morphometry MRI studies.
FWHM 12mm, FDR corrected at p < 0.05
13 studies, N = 2457
Regions were much smaller and more discrete;
Left putamen: Talairach coordinates (-38, 0, 16), Voxel cluster size 1248mm3, p < 0.01
Right putamen: Talairach coordinates (28, 6, 2), Voxel cluster size 464mm3, p < 0.01
Right head of caudate: Talairach coordinates (8, 0, 4), Voxel cluster size 424mm3, p < 0.01
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Basal ganglia
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Kambeitz J, Abi-Dargham A, Kapur S, Howes OD
Alterations in cortical and extrastriatal subcortical dopamine function in schizophrenia: Systematic review and meta-analysis of imaging studies
British Journal of Psychiatry 2014; 204(6): 240-249
View review abstract online
Comparison Cortical and extrastriatal D2/D3 receptor availability (measured by PET or SPECT) in unmedicated people with schizophrenia vs. controls.
Summary of evidence Moderate to low quality evidence (medium-sized samples, inconsistent, imprecise, direct) suggests no differences in D2/D3 receptor availability in the substantia nigra.
D2/D3 receptor availability
Binding potential relative to the non-displaceable compartment
Substantia nigra
No significant differences between groups in D2/D3 receptor availability;
5 studies, N = 143, d = 0.04, 95%CI -0.92 to 0.99, p = 0.90, I2 = 85%
Excluding one study of drug-naïve patients did not substantially change the effect (d = -0.04).
Meta-regression showed no effect of publication year, gender, or age in any analysis.
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Basal ganglia
Lahuis B, Kemner C, Van Engeland H
Magnetic resonance imaging studies on autism and childhood-onset schizophrenia in children and adolescents – a review
Acta Neuropsychiatrica 2003; 15(3): 140-147
View review abstract online
Comparison Brain volume in childhood-onset schizophrenia (COS) vs. healthy controls.
Summary of evidence Moderate to low quality evidence suggests child-onset schizophrenia patients exhibit increased volume in the basal ganglia.
Basal ganglia volume
12 studies, N unclear
Increased volume was observed in the caudate, putamen, and globus pallidus.
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Leung M, Cheung C, Yu K, Yip B, Sham P, Li Q, Chua S, McAlonan G
Gray Matter in First-Episode Schizophrenia Before and After Antipsychotic Drug Treatment. Anatomical Likelihood Estimation Meta-analyses With Sample Size Weighting
Schizophrenia Bulletin 2011; 37(1): 199-211
View review abstract online
Comparison Grey matter changes in people with first-episode schizophrenia
(treated and medication naïve) vs. healthy controls.
Summary of evidence Moderate quality evidence (large sample sizes, indirect, unable to
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Basal ganglia
assess consistency or precision) suggests greater reduction in the bilateral caudate in treatment naïve first episode schizophrenia patients compared to healthy controls and treated patients.
Basal ganglia volume
Meta-analysis was performed using Anatomical Likelihood Estimate (ALE) analysis on Voxel-Based Morphometry MRI studies.
FWHM 8mm, FDR corrected at p <0.05
6 studies, N = 327
Treatment naïve first-episode psychosis
Right caudate: Talairach coordinates (10, 10, 12), cluster 1936mm3, ALE 0.0019
Left caudate: Talairach coordinates (0, 12, 4), cluster 1936mm3, ALE 0.0057
Regions where grey matter reductions were larger in magnitude in treatment naïve patients than in
treated patients;
Right caudate: Talairach coordinates (10, 10, 12), cluster 1992mm3, ALE 0.0106
Left caudate: Talairach coordinates (0, 12, 4), cluster 360mm3, ALE 0.0276
Left caudate: Talairach coordinates (-12, 6, 0), cluster 264mm3, ALE 0.0095
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct for within group comparison, indirect for between group
comparison
MacDonald AW, Thermenos HW, Barch DM, Seidman LJ
Imaging genetic liability to schizophrenia: systematic review of FMRI studies of patients' nonpsychotic relatives
Schizophrenia Bulletin 2009; 35(6): 1142-1162
View review abstract online
Comparison Functional activation in first-degree relatives of people with schizophrenia vs. healthy controls.
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Basal ganglia
Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia
Archives of General Psychiatry 2009; 66(8): 811-822
View review abstract online
Comparison 1 Functional activation in individuals with schizophrenia vs. healthy controls: ALE analysis
Note – The claustrum is considered by some sources to be a part of the basal ganglia.
Summary of evidence Moderate quality evidence (large sample size, direct, unable to assess precision or consistency) suggests patients with schizophrenia show reduced activity in the bilateral claustrum and the right putamen during executive function tasks
Activation following executive function tasks: where controls have > activity than patients
with schizophrenia
Meta-analysis results reported for 41 studies of either fMRI or PET during executive function tasks.
41 studies, N = 1217
ALE analysis – FWHM 12mm, False Discovery Rate (FDR) corrected model
Significantly reduced activity in schizophrenia patients compared to controls
Right claustrum: Talairach centre of mass (26, 22, 2), cluster volume 1766mm3
Left claustrum: Talairach centre of mass (-28, 24, 0), cluster volume 880mm3
Right putamen: Talairach centre of mass (20, -4, 14), cluster volume 448mm3
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Navari S, Dazzan P
Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings.
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Basal ganglia
Summary of evidence High quality evidence (large sample sizes, consistent, precise, direct) suggests significantly greater reductions over time in the left caudate in people with schizophrenia.
Grey matter volume
Progressive changes in grey matter volume reported across longitudinal MRI scans over 1-10 years.
31 studies, N = 1867
Significant, small effect of greater reductions over time in schizophrenia compared to controls;
Left Caudate: N = 253, 3 studies, d = -0.336, 95%CI -0.60 to -0.07, p = 0.013, I2 = 0%
No differences between groups;
Right Caudate: N = 253, 3 studies, d = -0.132, 95%CI -0.49 to 0.23, p = 0.470, I2 = 41.6%
Consistency in results Consistent
Precision in results Precise
Directness of results Direct
Smieskova R, Fusar-Poli P, Allen P, Bendfeldt K, Stieglitz RD, Drewe J, Radue E W, McGuire PK, Riecher-Rossler A, Borgwardt SJ
The Effects of Antipsychotics on the Brain: What Have We Learnt from Structural Imaging of Schizophrenia? - A Systematic Review
Current Pharmaceutical Design 2009; 15(22): 2535-2549
View review abstract online
Comparison Grey matter volume changes in cross-sectional and longitudinal
assessments in treated and untreated people with schizophrenia
compared to healthy controls.
Summary of evidence Moderate to low quality evidence (unclear sample size, direct,
unable to assess consistency or precision) is largely unclear as
to the role of medication in mediating structural alterations in
people with schizophrenia.
Atypical antipsychotic medications appear broadly to be
associated with less structural alterations than typical
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Basal ganglia
Neuropsychopharmacology 2005; 30(11): 1949-1962
View review abstract online
Comparison Metabolic N-acetylaspartate amino acid (NAA) activity (measured by 1H-MRS) in grey matter regions in people with schizophrenia vs. healthy controls.
Summary of evidence Low quality evidence (sample size unclear, direct inconsistent, unable to assess precision) is unclear of NAA levels in the striatum of people with schizophrenia compared to controls.
NAA levels in grey matter regions
6 studies consider NAA, N unclear
Patient average 98.5% of control levels
Lenticular nucleus (putamen + globus pallidus)
2 studies consider NAA, N unclear
Patient average 104.5% of control levels
Caudate nucleus
3 studies consider NAA, N unclear
Patient average 100.3% of control levels
Putamen
7 studies consider NAA, N unclear
Patient average 100.6% of control levels
Striatum (caudate+putamen)
1 study considers NAA, N unclear
Patient average 112.6% of control levels
Consistency in results Inconsistent - significant heterogeneity reported, p < 0.0001.
Precision in results No confidence intervals are provided.
Directness of results Direct
Stone JM, Davis JM, Leucht S, Pilowsky LS
Cortical dopamine D2/D3 receptors are a common site of action for antipsychotic drugs--an original patient data meta-analysis of the SPECT
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Basal ganglia
Summary of evidence Moderate to low quality evidence (direct, unable to fully assess precision or consistency – data appears inconsistent) suggests bilateral caudate nucleus is significantly reduced in drug naive first episode psychosis patients compared to healthy controls.
Bilateral caudate nucleus volume
7 studies, N = 212
4 of 7 studies reported consistently reduced volume in bilateral caudate nucleus in patients.
3 of 7 studies reported no significant difference in caudate nucleus volume, although 2 of the 3 had
methodological limitations.
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Comparison 2 Cross-sectional comparison of medicated first episode psychosis patients (maximum 12 week treatment with first or second generation antipsychotics) compared to healthy controls.
Summary of evidence Moderate quality evidence (large sample size, direct, unable to fully assess precision or consistency – data appears consistent) suggests no significant difference in bilateral caudate volume in medicated first episode psychosis patients compared to healthy controls.
Bilateral caudate nucleus volume
4 studies, N = 428
4 of 4 studies reported no significant difference in bilateral caudate nucleus volume.
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Comparison 3 Longitudinal comparison of medicated first episode psychosis patients compared to healthy controls, measured at several varying time points.
Summary of evidence Moderate quality evidence (large sample size, direct, unable to fully assess precision or consistency – data appears consistent)
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Basal ganglia
suggests no significant difference in bilateral caudate volume over time in medicated first episode psychosis patients compared to healthy controls.
Bilateral caudate nucleus volume
6 studies, N = 548
6 of 6 studies reported no significant difference in overall bilateral caudate nucleus volume.
Consistency in results No measure of consistency is reported.
Precision in results No confidence intervals are provided.
Directness of results Direct
Wright IC, Rabe-Hesketh S, Woodruff PW, David AS, Murray RM, Bullmore ET
Meta-analysis of regional brain volumes in schizophrenia
American Journal of Psychiatry 2000; 157(1): 16-25
View review abstract online
Comparison Brain volume in people with schizophrenia vs. healthy controls.
Summary of evidence High quality evidence (large sample size, consistent, precise, direct) suggests increased right caudate, right putamen, and globus pallidus volume in people with schizophrenia compared to healthy controls.
Basal ganglia volume
Left caudate
No effect – average volume of schizophrenia caudate 101% of control volume, 95%CI 97% to 106%;
10 studies, N = 565, d = 0.06, no CIs reported, p = 0.01
Right caudate
Small effect size, average volume of schizophrenia caudate 99% of control volume, 95%CI 95% to 103%;
10 studies, N = 565, d = -0.06, no CIs reported, p = 0.02
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Basal ganglia
References
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3. Kambeitz J, Abi-Dargham A, Kapur S, Howes OD. Alterations in cortical and extrastriatal subcortical dopamine function in schizophrenia: Systematic review and meta-analysis of imaging studies. British Journal of Psychiatry. 2014; 204(6): 420-9.
4. Glahn DC, Laird AR, Ellison-Wright I, Thelen SM, Robinson JL, Lancaster JL, Bullmore E, Fox PT. Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biological Psychiatry. 2008; 64(9): 774-81.
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9. Steen RG, Hamer RM, Lieberman JA. Measurement of brain metabolites by 1H magnetic resonance spectroscopy in patients with schizophrenia: a systematic review and meta-analysis. Neuropsychopharmacology. 2005; 30(11): 1949-62.
10. Taylor H, Ricciardi A, Dazzan P. A review of caudate nucleus volume in first episode psychosis. Clinical Neuropsychiatry. 2007; 4(5-6): 191-8.
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12. Navari S, Dazzan P. Do antipsychotic drugs affect brain structure? A systematic and critical review of MRI findings. Psychological Medicine. 2009; 39(11): 1763-77.
13. MacDonald AW, 3rd, Thermenos HW, Barch DM, Seidman LJ. Imaging genetic liability to schizophrenia: systematic review of FMRI studies of patients' nonpsychotic relatives. Schizophrenia Bulletin. 2009; 35(6): 1142-62.
14. Stone JM, Davis JM, Leucht S, Pilowsky LS. Cortical dopamine D2/D3 receptors are a common site of action for antipsychotic drugs--an original patient data meta-analysis of the SPECT and PET in vivo receptor imaging literature. Schizophrenia Bulletin. 2009; 35(4): 789-97.
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16. Chan RCK, Di X, McAlonan GM, Gong Q-y. Brain Anatomical Abnormalities in High-Risk Individuals, First-Episode, and Chronic Schizophrenia: An Activation Likelihood Estimation Meta-analysis of Illness Progression. Schizophrenia Bulletin. 2009.
17. Leung M, Cheung C, Yu K, Yip B, Sham P, Li Q, Chua S, McAlonan G. Gray Matter in First-Episode Schizophrenia Before and After Antipsychotic Drug Treatment. Anatomical Likelihood Estimation Meta-analyses With Sample Size Weighting. Schizophrenia Bulletin. 2009.
18. Smieskova R, Fusar-Poli P, Allen P, Bendfeldt K, Stieglitz RD, Drewe J, Radue EW, McGuire PK, Riecher-Rossler A, Borgwardt SJ. The Effects of Antipsychotics on the Brain: What Have We Learnt
To donate, phone 1800 888 019 or visit www.neura.edu.au/donate/schizophrenia
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from Structural Imaging of Schizophrenia? - A Systematic Review. Current Pharmaceutical Design. 2009; 15(22): 2535-49.
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