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Structural Imaging and Neuroanatomy Research Unit

DIRECTOR: NANCY C. ANDREASEN, M.D., PH.D.
CO-DIRECTORS: MICHAEL VANNIER, M.D., JAMES EHRHARDT, Ph.D.

OVERALL AIMS
BACKGROUND AND RATIONALE
PROGRESS REPORT
PROGRESS WITH THE STUDY OF ANATOMIC/CIRCUIT ABNORMALITIES IN SCHIZOPHRENIA USING MR
PROJECTS
REFERENCES


Overall Aims
1. To use MR to identify and study the neuroanatomic abnormalities that occur in disease states, such as schizophrenia or autism.
2. To use MR to examine neuroanatomic measures that may provide information about neurodevelopmental processes, such as gyrification patterns.
3. To use MR to study and measure specific subregions hypothesized to be involved in dysfunctional anatomic/functional circuitry in schizophrenia, such as prefrontal cortex, thalamus, and cerebellum.
4. To use MR to examine anatomic circuitry directly through the use of diffusion anisotropy.
5. To use MR to study factors that could confound measurements of brain structure in schizophrenia, such as hydrational status.
6. To identify and develop new methods that will facilitate these aims, such as novel scanning sequences or new approaches to image analysis (e.g., neural nets, global pattern matching).
7. To confirm MR findings and improve their spatial resolution through the study of postmortem tissue.

Background and Rationale
The development of the technology of in vivo brain imaging during the past 15 years has provided an extraordinarily powerful group of tools for understanding the human brain. These tools permit us to study brain anatomy in exquisite detail, to observe shifts in metabolic activity as the brain responds to cognitive or perceptual challenges, and to quantitatively measure the neurochemical activity of a variety of neurotransmitter systems. Prior to the development of in vivo brain imaging, investigators were limited to indirect inferential techniques such as cognitive tests, the study of peripheral metabolites, or the examination of postmortem tissue. These earlier techniques imposed substantial technical limitations on investigations, making it difficult to disentangle the effects of aging and medication or interactions between the peripheral and central nervous system. In vivo brain imaging techniques allow us to study the human brain directly in both normal individuals and in patients suffering from major mental illnesses. These techniques offer the possibility of being able to identify the anatomic and physiologic substrates of these illnesses.

Our own work and that of others has repeatedly demonstrated that patients with schizophrenia have structural brain abnormalities (e.g., Johnstone et al 1976; Weinberger et al 1979, 1980b, 1988; Andreasen et al 1982d, 1986d, 1990b, 1994i; and many, many more). The challenge currently facing investigators in psychiatry is to build on the burgeoning knowledge base in basic neuroscience and the explosion in imaging and computer science technology in order to choose from a large array of hypotheses and techniques the ones that are most likely to advance our understanding of the normal brain and of major mental illnesses.

Proposed MR studies involve the examination of a series of scientific questions in cognitive neuroscience, systems level and developmental neurobiology, and clinical psychopathology. The studies focus on regions hypothesized to be important parts of the neural circuitry used in the cognitive processes that are dysfunctional in schizophrenia and other developmental disorders with shared phenomenology such as autism. Methods and regions have been chosen for study because they may elucidate this circuitry and the developmental processes that shape it from fetal life through young adulthood. Neurodevelopmental abnormalities have been an important working hypothesis for the mechanisms that produce schizophenia for many years (Feinberg, 1982, Andreasen et al 1986a, 1986d; Weinberger, 1987; Swayze et al 1990). Our more recent work, using both MR and PET, has led us to postulate that abnormal neurodevelopmental mechanisms may preferentially affect the connectivity between midline regions, such as the thalamus, and cortical regions, leading to impairment in the ability to fluidly coordinate mental activities (Andreasen et al 1996k, 1997g, in press a).

The projects in this research unit are designed to illuminate various facets of this hypothesis. Seven projects are included. The first project continues our ongoing work to examine the neuroanatomic substrates of schizophrenia using MR, with an emphasis on examining specific nodes on the CCTCC. The second project tackles the difficult problem of measuring thalamic subnuclei in detail: developing a new scanning sequence and examining the reliability and validity of this new approach to visualization and measurement. The third project extends the investigation of the thalamus in schizophrenia to the cellular and molecular level, through a study that will use postmortem tissue to examine region-specific alterations in cell number and neurotransmitter distribution in the dorsal thalamus. The fourth project uses MR to examine a childhood-onset neurodevelopmental disorder, autism, employing measurements similar to those used in our adult schizophrenic sample, in order to identify patterns of anomalous organization and connectivity. The fifth project proposes to use cutting edge MR image analysis techniques in order to examine brain development in children and adolescents and to study individual variability due to gender effects, handedness, or laterality. The sixth project employs a specific new MR technique, anisotropic diffusion imaging, to directly examine the connectivity of brain regions in vivo and compare prefrontal-cerebellar-thalamic circuitry in patients with schizophrenia and normal controls. The seventh project conducts experimental studies designed to examine one potential confounder of structural MR measurements, hydration status, within the context of several studies that we have already conducted to date that indicate that anatomic measures are not static and that they may be changed by exogenous factors such as exposure to neuroleptic medication (Rodriguez et al submitted; Swayze et al 1992; Westmoreland et al submitted).

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Progress Report
This research unit has made substantial progress over the past four years. While external grant support is only an indirect indicator of achievement, nonetheless it is an important one. In our last application, only one project in the MR Research Unit (as this unit was then named) had external support. In this application, five of the seven projects have external funding. Two others are promising pilot projects for which we request seed money support so that external funding can be obtained. More importantly, however, this unit has also made substantive scientific progress. In the previous review, reviewers were concerned that the proposed studies lacked a unifying and innovative group of hypotheses to be tested. Our work completed during the past four years--combining image analysis techniques with MR and PET findings--has permitted us to clearly articulate a major direction and some heuristic hypotheses that we believe likely to advance knowledge about the mechanisms of schizophrenia. Our MR studies have provided an important group of findings that support conceptualizing schizophrenia as a neurodevelopmental disorder that is due to dysfunctional neural circuits (and specifically the CCTCC). Further, some of our results suggest that the abnormality may be structural in addition to metabolic/physiologic/neurochemical. The studies proposed for the coming five years follow up on these findings in various ways. One of our two pilot studies uses the substantial expertise of Martin Cassell to examine the neuropathology of thalamic subnuclei (Project 3), while the other extends MR technology to in vivo study of neuronal connectivity through anisotropic diffusion imaging (Project 6). Other studies propose to use structural MR to examine nodes on the CCTCC and to use gyrification measures to examine brain development (Projects 1 and 2), to examine structural abnormalities in a related neurodevelopmental disorder, autism (Project 4), to study neurodevelopment and gender differences in normals (Project 5), and to examine the effects of hydration on measurement of brain structure (Project 7).

Much of the progress achieved to date has depended on the continuing development of new and powerful methods for simplifying and automating the process of measuring and analyzing MR data, through the further development of our software package, BRAINS. Some of this progress is summarized in the Image Analysis Core Unit, which outlines the various tools available in BRAINS and describes our work to date in assessing their reliability and validity. Briefly, our progress with image analysis includes the development of:
Volume rendering software that permits simultaneous visualization of anatomy in three orthogonal planes and visualization of brain surface anatomy, tracing on either brain surface or internal structures, telegraphing of the coordinates across the other portions of the image to produce very accurate measurement of structures based on simultaneous three-dimensional visualization, and calculation of areas and volumes of the structures/regions traced.
Standard and reliable methods for manually tracing individual brain structures or regions, such as lobes of the brain, the hippocampus, or the caudate nucleus.
Automated atlas-based methods for subdividing the brain into specific lobes.
Both linear and nonlinear methods for normalizing brains so that subjects can be averaged and so that both subcortical and gyral anatomy can be made as comparable as possible across individuals.
Methods to measure differences in the shape of brain subregions (similar to the thin plate spline technique).
Multispectral methods for achieving precise segmentation of brain tissue into gray matter (GM), white matter (WM), and cerebrospinal fluid (CSF).
Image subtraction techniques as a tool for doing cross-group comparisons of differences.
Methods for visualizing and measuring sulcal and gyral anatomy, including validation.

These various methods, which are the consequence of many years of effort in developing well-validated and accurate methods for measuring brain anatomy, are nearly all completely automated. Having automated methods produces many advantages. It permits the study of large samples with relative speed and efficiency. It eliminates laborious hand-tracing, which is not only time-consuming, but also requires careful calibration across tracers and can potentially be less reliable if rater drift occurs.

The techniques to measure surface anatomy were particularly difficult to achieve, since they required that we solve some of the fundamental problems in finding an accurate brain surface, such as "touching gyri" and "buried cortex." We now have, however, a valid and sensitive group of measures of gyrification, including a classic Zilles gyrification index, a 3D adaptation of it, a measure of brain surface area, a measure of cortical thickness for the entire surface, and measures of the degree of sulcal and gyral curvature. These measures will assist us in using indices of gyrification as a tool to probe neurodevelopmental abnormalities.

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Progress with the Study of Anatomic/Circuit Abnormalities in Schizophrenia Using MR
Our progress in this area includes finding:


These findings provide convergent evidence from multiple structural imaging studies that patients with schizophrenia have measurable abnormalities in the nodes in the CCTCC. Nonetheless, methods used to date are relatively crude, since we have only measured large regions or structures that are known to have important anatomical and functional subdivisions. Consequently, our future structural MR studies of schizophrenia will focus on the development and application of more fine-grained methods for conducting anatomic measurements of the prefrontal cortex, the cerebellum, and the thalamus.


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