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Meta-Analysis of 41 Functional Neuroimaging Studies of Executive Function in Schizophrenia

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Meta-Analysis of 41 Functional Neuroimaging Studies of Executive Function in Schizophrenia META-ANALYSIS Meta-analysis of 41 Functional Neuroimaging Studies of Executive Function in Schizophrenia Michael J. Minzenberg, MD; Angela R. Laird, PhD; Sarah Thelen, BS; Cameron S. Carter, MD; David C. Glahn, PhD Context: Prefrontal cortical dysfunction is frequently re- with statistical thresholding and correction for multiple ported in schizophrenia. It remains unclear whether this comparisons. represents the coincidence of several prefrontal region- and process-specific impairments or a more unitary dysfunc- Data Synthesis: In within-group analyses, healthy con- tion in a superordinate cognitive control network. Whether trols and patients activated a similarly distributed cortical- these impairments are properly considered reflective of hy- subcortical network, prominently including the dorsolat- pofrontality vs hyperfrontality remains unresolved. eral prefrontal cortex (PFC), ventrolateral PFC, anterior cingulate cortex (ACC), and thalamus. In between-group Objectives: To test whether common nodes of the cog- analyses, patients showed reduced activation in the left dor- nitive control network exhibit altered activity across func- solateral PFC, rostral/dorsal ACC, left thalamus (with sig- tional neuroimaging studies of executive cognition in schizo- nificant co-occurrence of these areas), and inferior/ phrenia and to evaluate the direction of these effects. posterior cortical areas. Increased activation was observed in several midline cortical areas. Activation within groups Data Sources: PubMed database. varied modestly by task. Study Selection: Forty-one English-language, peer- Conclusions: Healthy adults and schizophrenic patients reviewed articles published prior to February 2007 were activate a qualitatively similar neural network during ex- included. All reports used functional neuroimaging dur- ecutive task performance, consistent with the engagement ing executive function performance by adult patients with of a general-purpose cognitive control network, with criti- schizophrenia and reported whole-brain analyses in stan- cal nodes in the dorsolateral PFC and ACC. Nevertheless, dard stereotactic space. Tasks primarily included the de- patients with schizophrenia show altered activity with defi- layed match-to-sample, N-back, AX-CPT, and Stroop tasks. cits in the dorsolateral PFC, ACC, and mediodorsal nucleus of the thalamus. Increases in activity are evident in other Data Extraction: Activation likelihood estimation PFC areas, which could be compensatory in nature. modeling reported activation maxima as the center of a 3-dimensional gaussian function in the meta-analysis, Arch Gen Psychiatry. 2009;66(8):811-822 MPAIRED COGNITION IS A CORE, as the ventrolateral PFC (VLPFC), dorso- disabling feature of schizophre- lateral PFC (DLPFC), ventromedial PFC, nia, with no established treat- and anterior cingulate cortex (ACC). A re- ment. Although numerous defi- cent quantitative meta-analysis of 12 N- Author Affiliations: cits have been described across back studies found alterations among Department of Psychiatry, Iperceptual, attentional, mnemonic, lin- schizophrenic subjects compared with University of California–Davis guistic, and intellectual functions, im- healthy controls in several nodes of this School of Medicine, Sacramento paired executive functions are among the neural network, including reduced activ- (Drs Minzenberg and Carter); most widely observed, and they are con- ity in the DLPFC and increased activity in Research Imaging Center, sistently associated with impaired func- the VLPFC , ACC, and left frontal pole.2 University of Texas Health tion of the prefrontal cortex (PFC).1 Dif- Other studies have reported reduced ac- Science Center at San Antonio, ferent aspects of executive dysfunction tivity in the VLPFC during other work- San Antonio (Dr Laird and have been examined, including multiple ing memory tasks3 and in the ACC dur- Ms Thelen); and Department of 4,5 Psychiatry, Yale University facets of working memory, response in- ing conflict processing. School of Medicine, hibition, conflict processing, and prob- One possible interpretation of these New Haven, Connecticut lem solving, demonstrating deficits across findings is that there is a general deficit in (Dr Glahn). a range of circumscribed PFC regions, such PFC function in schizophrenia, with find- (REPRINTED) ARCH GEN PSYCHIATRY/ VOL 66 (NO. 8), AUG 2009 WWW.ARCHGENPSYCHIATRY.COM 811 ©2009 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 ings in a given task reflecting a distinct underlying cir- METHODS cuitry that supports each particular function, eg, the VLPFC for working memory maintenance, the DLPFC STUDY SELECTION for working memory manipulation or interference con- trol, and the frontopolar cortex for response inhibition. A PubMed literature search was performed to identify English- Alternatively, there could be a set of regions that show language, peer-reviewed studies that investigated executive func- impaired function in schizophrenia across a range of tasks tion in schizophrenic patients and healthy control subjects using and other areas with preserved or compensatory func- functional magnetic resonance imaging or positron emission tion. One hypothesis suggests that there is impaired tomography. Executive functions can be defined as processes DLPFC activity in the presence of an intact VLPFC.6 To- necessary to control or regulate other cognitive processes in the service of goal-directed behavior. The term cognitive con- gether with reports of selective loss of neuropil in dorsal trol is often used to describe executive functions to emphasize vs ventral regions of the PFC, this hypothesis might im- the regulatory component of this aspect of information pro- ply some subregion specificity to frontal dysfunction, ie, cessing. For this analysis, we searched for studies that used task the DLPFC is impaired while the VLPFC is not. An in- paradigms that are typically associated with executive func- fluential model of PFC function assigns the dorsolateral tions or cognitive control. These included delayed match-to- regions a critical superordinate role in regulating cogni- sample or delayed response (including Sternberg item recog- tive control.7 According to this model, the DLPFC main- nition), go/no-go (including AX-CPT), mental arithmetic, tains the context or task set to ensure accurate and flex- N-back, oddball, sequence recall, Stroop, Wisconsin Card Sort, and word generation tasks. Studies that did not report results ible performance during higher-level cognition, while as 3-dimensional coordinates in standard stereotactic space or medial frontal regions (eg, the ACC) support dynamic that reported only data from individual subjects or deactiva- 8,9 adjustments in control in concert with the DLPFC. Ac- tions were excluded. Forty-one studies published prior to Feb- cording to this view, dysfunction in general-purpose, high- ruary 2007 met these criteria (Table 1).3,5,13-51 Study design level cognitive control functions of the dorsolateral and features are indicated in Table 1, including clinical character- medial PFC could result in a wide range of deficits in dif- istics like illness duration and symptom severity; sex ratio among ferent executive functions in schizophrenia. the patient group; medication status; block vs event-related de- In this article, we use meta-analysis to test whether sign; and performance-matched vs nonmatched groups for analy- the various executive function deficits observed across sis. From this group of studies, coordinate results of within- group activations and between-group differences were divided functional neuroimaging studies in schizophrenia rep- into 4 groups: activations in schizophrenic patients, activa- resent the coincidence of several PFC subregion- and task- tions in normal control subjects, increases in schizophrenic pa- specific dysfunctions or a more unitary dysfunction of a tients relative to controls, and increases in controls relative to general-purpose, DLPFC/ACC-based cognitive control schizophrenic patients. To evaluate potential task-specific pat- network. In this context, the meta-analytic approach is terns of activation, we also repeated the within-group analy- uniquely valuable, as it allows us to test a research prob- ses in an identical manner but with the subsets of studies seg- lem that is not easily addressed in a single study; to over- regated by task type. come equivocation or inconsistencies in an existing lit- erature; and to provide the reader with the landscape of ACTIVATION LIKELIHOOD ESTIMATION a research domain, which in contemporary biomedical Activation likelihood estimation meta-analysis was con- research may be more highly valued than the results of 11,52 10 ducted. All data processing was performed in the BrainMap an individual study. Activation likelihood estimation environment.53,54 On insertion into the database, the spatial nor- (ALE) is a meta-analytic tool that models 3-dimen- malization template of each article was noted and the coordi- sional coordinates (from reported activations in a stan- nates were automatically transformed to allow analysis relative dard space) as the center of a 3-dimensional gaussian dis- to a single template.55 Coordinates were converted using the tribution.11 This obviates the need for raw data and thus icbm2tal transformation,56 which has shown to provide im- 57 increases the potential set of studies subject to meta- proved fit over the mni2tal transformation. Included
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