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An Expanded Role for Functional Neuroimaging in Schizophrenia Joseph H Callicott

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An Expanded Role for Functional Neuroimaging in Schizophrenia Joseph H Callicott 256 An expanded role for functional neuroimaging in schizophrenia Joseph H Callicott Functional magnetic resonance imaging is a surprisingly versatile at hand. Perhaps the most promising development in tool in the quest for disentangling the complexities of mental neuroimaging of schizophrenia has been the expansion illnesses such as schizophrenia. Yet, the identification of of functional brain imaging into the characterization of pathognomonic physiological features of the illness or even a intermediate phenotypes for psychiatric genetics studies. consensus regarding the interpretation of reported findings The intermediate phenotype attempts to quantify a phy- remain unfulfilled goals, in spite of the increasing sophistication siological aspect of a given illness, analogous to the of this technology. Nonetheless, by providing quantification of quantification of blood glucose in diabetes, which impacts brain function during various cognitive challenges, functional on the overall susceptibility to the illness but that carries a MRI has been used to leap ahead of these quandaries to identify simpler physiological basis and, hopefully, genetic archi- relationships between genetic variation and brain function. By tecture. As the heritability of mental illnesses such as examining recent findings and efforts to link these findings to schizophrenia is complex this approach is particularly genes, this article will review these exciting developments in attractive, especially given the frustratingly slow progress schizophrenia research. of linkage studies that have used the clinical phenotype as a starting point. Addresses Unit on Functional MRI Clinical Brain Disorders, Branch NIMH/NIH, Here, I summarize recent findings from the functional Building 10, Room 4D-20, MSC 1389 Bethesda, MD 20892-1389, USA neuroimaging literature in schizophrenia as a means of e-mail: [email protected] identifying candidate phenotypes. Finally, I discuss recent attempts to define specific genetic abnormalities Current Opinion in Neurobiology 2003, 13:256–260 that are associated with functional intermediate pheno- types. Though issues such as susceptibility to movement This review comes from a themed issue on Cognitive neuroscience artefact and controversial study design remain to be Edited by Brian Wandell and Anthony Movshon overcome, functional neuroimaging is poised to make revolutionary contributions towards uncovering the etiol- 0959-4388/03/$ – see front matter ogy of major mental illnesses such as schizophrenia. This Published by Elsevier Science Ltd. progress will be possible largely because of the non- DOI 10.1016/S0959-4388(03)00041-2 invasive nature of functional neuroimaging and the ease with which large numbers of subjects for this technique can be accumulated. Abbreviations COMT catechol-O-methyl transferase DLPFC dorsolateral prefrontal cortex Intermediate phenotypes in schizophrenia DZ dizygotic The search for brain-imaging phenotypes of schizophrenia fMRI functional magnetic resonance imaging has been underway since seminal studies in structural met methionine MZ monozygotic brain imaging were carried out during the late 1970s val valine and early 1980s (for a review see [1]). Early computerized VBR ventricle-to-brain ratio tomography (CT) studies showed that lateral ventricular WM working memory enlargement, or ventriculomegaly, was a replicable and robust group finding. Johnstone et al. [2] examined both 17 elderly institutionalized patients with schizophrenia and Introduction matched controls using CT. The patients as a group had Though only ten years old, functional magnetic reso- larger ventricles and, at the level of the individual patient, nance imaging (fMRI) has had a dramatic impact on ventriculomegaly predicted the extent of cognitive impair- the study of mental illness. A complete review of recent ment. This study suggested that the phenotype could be developments in the imaging of mental illness is beyond defined in a meaningful fashion at the individual level. It the scope of this article, whereas a review of recent only remained to be determined if the lateral ventriculo- progress in the study of schizophrenia is worthwhile. This megaly phenotype was heritable within families afflicted is because work with schizophrenia often provides a by schizophrenia. Taken together, the results of three template upon which researchers base their approach seminal studies showed just this. Weinberger et al. [3] to other mental illnesses. In the past two years, the compared the distribution of lateral ventriculomegaly in sequencing of the human genome has raised expectations seven healthy pairs of siblings, or sibships, with that in that the identification of susceptibility genes for the major nine sibships in which at least one member had schizo- psychiatric disorders such as schizophrenia should be near phrenia. Ventricle-to-brain ratio (VBR) was examined as a Current Opinion in Neurobiology 2003, 13:256–260 www.current-opinion.com Functional neuroimaging in schizophrenia Callicott 257 putative heritable phenotype in two ways: first, quantita- dysfunction, and whether functional findings arise as a tively by intra-class correlation of VBR within sibships, result of the schizophrenia or as a consequence of poor and second, qualitatively with scatterplots that compared performance on the cognitive tasks that are used to probe the VBR of any given individual to an established mean subjects. Several recent fMRI studies raise the question VBR in controls. Both analyses suggested that VBR was of whether widespread global dysfunction arises in schi- heritable. Reveley and co-workers [4] addressed the same zophrenics using simple tasks that are designed to probe questions in monozygotic (MZ) and dizygotic (DZ) twins. the response to sensory input. Wible et al. [6] tested an Using the VBR, heritability was calculated between 11 auditory sensory mismatch paradigm in 10 schizophrenic pairs of healthy MZ twins, eight pairs of healthy DZ twins, patients and 10 controls. The subjects were required to and seven pairs of MZ twins that were discordant for identify deviant tones that occurred in a string of standard schizophrenia. The VBR was highly heritable in healthy tones. The researchers found that both groups activated MZ twins (h2 ¼ 0.98), and roughly twice that of healthy auditory processing regions in superior temporal gyrus, DZ twins (h2 ¼ 0.45). The VBR was also highly heritable but that schizophrenic patients showed a diminished in schizophrenic DZ twins (h2 ¼ 0.87). A strong family response. Although it is not known to what extent tem- history of psychosis (manifested either by frank schizo- poral cortex neurons are affected by schizophrenia, these phrenia or simply by family history) predicts a greater data suggest a fundamental neuronal dysfunction that is concordance for the phenotype in question within sib- likely to be present throughout sensory and association ships, as found by Weinberger et al. [3]. However, echoing cortices, and thus suggest a global defect. Kiehl and this apparent genetic loading effect, the two schizophrenic Liddle [7] used a more traditional auditory oddball task DZ sibships with a strong family history of psychosis in the in a comparison of 11 schizophrenic patients and 11 study by Reveley et al. [4] showed the least within-pair controls. Detection of the oddball activated a network variance. Finally, DeLisi and co-workers [5] demonstrated including the dorsolateral frontal cortex, the thalamus, the a significant familial component of lateral ventricular superior temporal gyri, the parietal cortex, and the cin- enlargement in 11 sibships (including non-psychotic sib- gulate gyrus. Once again, schizophrenic patients pro- lings of schizophrenic patients or so-called unaffected duced less activation in the superior temporal gyrus siblings), which was not entirely explained by non-genetic but also in the thalamus and the frontal, parietal, and or environmental factors, such as early head injury or cingulate cortices. These data clearly implicate higher obstetrical complications. Taken together, these studies association cortices in addition to sensory cortex dysfunc- suggested that one could answer both questions using tion in schizophrenia. Braus et al. [8] examined simple brain imaging — ventriculomegaly was under genetic sensory processing in medication-naı¨ve schizophrenic control and variation was not significantly affected by subjects. They used a flashing checkerboard and drum- non-genetic factors. However, following these early stu- beats as stimuli and found abnormally reduced activation dies, the study of intermediate phenotypes languished for in the prefrontal cortex, the thalamus, and the parietal nearly two decades. lobe, again implicating higher association cortices in schizophrenia. Kodama et al. [9] examined brain activa- In principle, a phenotype related to genetic risk should be tion in schizophrenic patients one week after they had found in all schizophrenic individuals, and in some ‘at undergone motor skills training and found, contrary to the risk’ individuals who do not manifest the symptoms. typical pattern of reduced and more-focused brain activa- Thus, the search for phenotypes at the level of brain tion in controls, that schizophrenic patients continued to imaging begins with patients who manifest schizophrenia. show increased activation. Kumari et al. [10] found that Although functional brain-imaging techniques have been schizophrenic patients failed to activate a network of applied to the study
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