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  • Review Article
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Towards multimodal atlases of the human brain

Nature Reviews Neuroscience volume 7, pages 952–966 (2006)Cite this article

Key Points

  • Brain atlases are reference systems that associate neuroanatomical labels (nomenclature) with canonical representations of anatomy in a three-dimensional coordinate system. These systems commonly integrate multisubject data from many different sources (for example, histology, functional MRI and positron emission tomography), and could provide statistical representations of anatomy and function in whole populations.

  • Initially, brain atlases were purely neuroanatomical, based on a single, often sparsely sampled, representative example. Now, brain atlases include population statistics on structure, gene expression, receptor patterns or connectivity over time.

  • Modern cytoarchitectonic studies are using computational methods to pool information across subjects on such features as receptor distributions, myelination characteristics and cellular content. Correlations between functional activation and the underlying cyto- or myeloarchitecture can then be tested by using these architectural maps to define regions of interest in functional imaging studies.

  • Integration of cytoarchitectural maps from many subjects has allowed classical maps to be re-evaluated and corrected. It has also led to a quantitative description of the intersubject variability of cytoarchitectonic areas and to the discovery of hitherto unknown cytoarchitectonic areas in the intraparietal, secondary somatosensory and extrastriate cortex.

  • Diffusion tensor imaging (DTI) provides a new source of image contrast to map white matter integrity and connectivity, and has opened up new opportunities for brain mapping and atlasing.

  • Population-based atlases can average anatomical features across individuals, revealing generic features that are not identifiable in individual representations owing to their considerable variability. They have identified group-specific patterns of brain structure in Alzheimer's disease, HIV/AIDS, schizophrenia, in methamphetamine users, and in developmental disorders such as fetal alcohol syndrome and Williams syndrome.

  • Brain atlases are beginning to be used in clinical studies, including drug trials of antipsychotics or mood stabilizers, to investigate factors that influence disease expression and therapeutic response.

  • In the next decade, population-based atlases will probably gain widespread applicability in genetic studies. Data from twins and those at genetic risk for specific diseases have been incorporated into brain atlasing studies to discover previously unknown effects on the brain of variations at specific genetic loci.

Abstract

Atlases of the human brain have an important impact on neuroscience. The emergence of ever more sophisticated imaging techniques, brain mapping methods and analytical strategies has the potential to revolutionize the concept of the brain atlas. Atlases can now combine data describing multiple aspects of brain structure or function at different scales from different subjects, yielding a truly integrative and comprehensive description of this organ. These integrative approaches have provided significant impetus for the human brain mapping initiatives, and have important applications in health and disease.

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Figure 1: Observer-independent procedure for cytoarchitectonic parcellations.
Figure 2: Summary of procedures for generating a multimodal probabilistic atlas.
Figure 3: Cytoarchitectonic probability maps of the cortex.
Figure 4: Correlation between receptor autoradiography and myeloarchitectonic borders.
Figure 5: Comparison of a conventional T1-weighted image and DTI-based contrasts.
Figure 6: Comparison between a post-mortem brain sample and the results of DTI-based three-dimensional tract reconstruction.
Figure 7: Examples of various methods of mapping the white matter based on DTI.
Figure 8: Brain atlases that represent specific subpopulations.

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Acknowledgements

This work was supported by research grants from the National Institutes of Health (NIH), Roadmap Initiative for Bioinformatics and Computational Biology, National Center for Research Resources, the National Institute of Mental Health (NIMH) and the National Institute of Neurological Disorders and Stroke, and by Human Brain Project grants to the International Consortium for Brain Mapping, funded jointly by NIMH and the National Institute on Drug Abuse and one funded by the National Institute of Aging (NIA). Additional support was provided by the National Institute for Biomedical Imaging and Bioengineering, the National Center for Research Resources and the NIA, the National Library of Medicine and the Biomedical Informatics Research Network (BIRN, http://www.nbirn.net), which is funded by the National Center for Research Resources at the NIH. Other funds came from the German Ministry of Science BMBF, the Helmholtz Association of Research Centres and from various grants from the German Research Foundation DFG and the European Union. We thank the many collaborators and doctoral students in our laboratories. Special thanks to P. Roland from the Karolinska Institute Stockholm for an exciting collaboration of many years, and to N. Palomero-Gallagher for her enthusiasm in the receptor project.

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Authors and Affiliations

  1. Department of Neurology, Laboratory of Neuro Imaging, UCLA School of Medicine, Los Angeles, California, USA

    Arthur W. Toga & Paul M. Thompson

  2. Department of Radiology and Radiological Science, Johns Hopkins University School of Medicine, Baltimore, 21205, Maryland, USA

    Susumu Mori

  3. Institute of Medicine and Brain Imaging Centre West (BICW), Research Centre Jülich, Germany

    Katrin Amunts & Karl Zilles

  4. Department of Psychiatry and Psychotherapy, RWTH Aachen University, Aachen, Germany

    Katrin Amunts

  5. C. & O. Vogt-Institute of Brain Research, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany

    Karl Zilles

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  1. Arthur W. Toga
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Correspondence to Arthur W. Toga.

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DATABASES

OMIM

Alzheimer's disease

autism

schizophrenia

Williams syndrome

FURTHER INFORMATION

Toga's laboratory

Alzheimer's Disease Neuroimaging Initiative

International Consortium for Brain Mapping

Statistical Parametric Mapping

Glossary

Cartographic approaches

Approaches that place brain images from multiple subjects and devices into an anatomical reference system with standardized three-dimensional coordinates (for volumetric images) or two-dimensional spherical or planar coordinates (for cortical regions).

Cytoarchitecture

Subdivisions (named or numbered) of the cerebral cortex, called cytoarchitectonic maps, based on cellular features (size and shape of cells, cell packing density in different cortical layers, width of layers) and identified in cell body-stained specimens.

Magnetic resonance imaging

(MRI). A non-invasive method to obtain images of living tissue. It uses radio-frequency pulses and magnetic field gradients; the principle of nuclear magnetic resonance is used to reconstruct images of tissue characteristics (for example, proton density, water diffusion parameters).

Multispectral characterization

Multispectral imaging devices measure multiple features of an object at each spatial location, such as optical reflectance at different wavelengths, or different relaxometric decay constants (T1 and T2) in MRI.

Chemoarchitectural maps

Differences in the molecular composition of cortical and subcortical brain regions can be assessed using enzyme- or immunohistochemistry, in situ hybridization, receptor autoradiography and so on, revealing subdivisions with distinctive distribution patterns, such as expression of transmitter receptors.

Diffusion tensor imaging

(DTI). A technique developed in the mid-1990s, based on MRI in which diffusion constants of water molecules are measured along many (>6) orientations and diffusion anisotropy is characterized. It is used to visualize the location, orientation and anisotropy of the brain's white matter tracts, and is sensitive to directional parameters of water diffusion in the brain.

Myeloarchitecture

Subdivisions (numbered or named) of the cerebral cortex, called myeloarchitectonic maps, based on features (for example, stria of Gennari in the visual cortex) of myelinization (differential density of myelinated fibres and fibre bundles in different cortical layers), and identified in myelin-stained histological specimens.

Stereotaxic system

A technique or apparatus used in neurosurgery or brain imaging studies to localize a specific anatomical locus using standardized three-dimensional coordinates; used, for example, for directing the tip of a surgical instrument (such as a needle or electrode) to a known location.

Functional imaging

Distinct from structural imaging techniques such as computerized tomography or MRI that assess anatomical structure, functional imaging techniques (for example, positron emission tomography, functional MRI and electroencephalography) are sensitive to physiological processes such as neuronal activation, electromagnetic properties of living tissue, blood flow or metabolism.

Multimodal association cortices

The multimodal association cortices of the parietal and frontal lobes integrate somatosensory, auditory and visual information for higher-order cognitive processing.

Positron emission tomography

A medical imaging technique that uses injected radiolabelled tracer compounds in conjunction with mathematical reconstruction methods to produce a three-dimensional image or map of functional processes in the body, such as glucose metabolism, blood flow or receptor distributions.

Multimodal microstructural approach

An approach to characterize fine-scale anatomy using multiple histological and neurochemical techniques, revealing different aspects of cellular organization or molecular composition.

Fibre-tracking approaches

Using this approach, three-dimensional trajectories of white matter tracts can be reconstructed. The algorithm is based on fibre orientation information obtained from diffusion tensor imaging.

Probability map

A map that depicts the likelihood of a particular feature. It can be used to show how frequently, in percentage, a given anatomical structure is found in a specific location across a population of subjects.

Cytoarchitectonic probability maps

Based on a sample of brains that have been parcellated using cytoarchitectonic criteria; they display the statistical likelihood, or relative frequency, that a particular voxel in stereotaxic space contains a given cytoarchitectonic unit (for example, a cortical area, or a subcortical nucleus).

Maximum probability maps

Summary maps in which each voxel of the three-dimensional space has been assigned to the cytoarchitectonically defined unit with the highest probability. They are calculated on the basis of probability maps, such as cytoarchitectonic probability maps, to generate a map with unambiguously defined borders.

Voxel

The three dimensional equivalent of a pixel. A pixel is a picture element, and a voxel is a volume element.

T1-weighted images

One of most widely used MRI methods, in which the contrast is based on a selection of MRI acquisition parameters, producing an image that weights signal by the relaxometric parameter, T1, of each tissue (that is, the longitudinal relaxation time). In the brain, T1-weighting causes fibre tracts (nerve connections) to appear white, cortex and basal nuclei to appear grey, and cerebrospinal fluid to appear dark.

Relaxometry

The measurement of relaxation parameters in nuclear MRI, such as the longitudinal (T1) or transverse (T2) decay constants that characterize signal decay from excited nuclei. By detecting subtle differences in relaxation times, relaxometry is capable of differentiating various tissue types in the brain.

Anisotropy map

The directional dependency of water diffusion at each point in the brain can be summarized using measures such as fractional anisotropy. High anisotropy values indicate heavily myelinated white matter, whereas decreased anisotropy is often a sign of disease.

Anisotropic diffusion

Diffusion of a substance (for example, water) that is greater in certain preferred directions, such as along the axons of a fibre tract.

Isotropic diffusion

Diffusion of a substance (for example, water) that is uniform in all directions.

Tensor-valued information

Information that can be modelled mathematically as a matrix, or tensor, at each location in an object. Diffusion tensor imaging produces signals with at least six independent parameters at each anatomical point (the diffusion tensor); tensor calculus can then be used to estimate diffusion parameters in any specific direction.

Partial volume effects

This refers to the blurring of intensity differentiations used to classify contributing tissue types (grey matter, white matter and cerebrospinal fluid). It is the results of pixels placed over a region that contains multiple tissue types. The smaller the pixel size the less frequently this is problematic.

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Toga, A., Thompson, P., Mori, S. et al. Towards multimodal atlases of the human brain. Nat Rev Neurosci 7, 952–966 (2006). https://doi.org/10.1038/nrn2012

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