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Microstructural Parcellation of the Human Cerebral Cortex – from Brodmann’S Post-Mortem Map to in Vivo Mapping with High-Field Magnetic Resonance Imaging

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Microstructural Parcellation of the Human Cerebral Cortex – from Brodmann’S Post-Mortem Map to in Vivo Mapping with High-Field Magnetic Resonance Imaging PERSPECTIVE ARTICLE published: 18 February 2011 HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2011.00019 Microstructural parcellation of the human cerebral cortex – from Brodmann’s post-mortem map to in vivo mapping with high-field magnetic resonance imaging Stefan Geyer*, Marcel Weiss, Katja Reimann, Gabriele Lohmann and Robert Turner Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany Edited by: The year 2009 marked the 100th anniversary of the publication of the famous brain map of Patrik Vuilleumier, University Medical Korbinian Brodmann. Although a “classic” guide to microanatomical parcellation of the cerebral Center and University Hospital Geneva, Switzerland cortex, it is – from today’s state-of-the-art neuroimaging perspective – problematic to use Reviewed by: Brodmann’s map as a structural guide to functional units in the cortex. In this article we discuss Katrin Amunts, Aachen University, some of the reasons, especially the problematic compatibility of the “post-mortem world” of Germany microstructural brain maps with the “in vivo world” of neuroimaging. We conclude with some *Correspondence: prospects for the future of in vivo structural brain mapping: a new approach which has the Stefan Geyer, Department of enormous potential to make direct correlations between microstructure and function in living Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, human brains: “in vivo Brodmann mapping” with high-field magnetic resonance imaging. Stephanstrasse 1a, 04103 Leipzig, Keywords: brain map, cortical areas, cytoarchitecture, myeloarchitecture, quantitative T1 map Germany. e-mail: [email protected] Around the turn of the twentieth century, several neuroanatomists, A major goal of Brodmann was to elucidate the evolutionary among them Alfred Walter Campbell, Grafton Elliot Smith, background of structural differentiation in the cortex. Hence, in Korbinian Brodmann, and Cécile and Oskar Vogt, set out to his monograph (for an English translation see Garey, 2006) he study the microanatomy of the human cerebral cortex. They published cytoarchitectonic maps of the cortex of Homo sapiens noticed that the laminar architectonic pattern of neurons in prep- and eight other mammals ranging from insectivores (Erinaceus arations stained for cell bodies (e.g., with the Nissl technique) europaeus or hedgehog) to non-human primates (Cercopithecus or and/or the arrangement of tangentially and radially oriented guenon). He found that some cortical areas, e.g., areas 4, 1, and 17 myelinated fibers in preparations stained for myelin sheaths are present in almost all species examined, whereas other regions (e.g., with the Weigert technique) are not uniform across the in the frontal, posterior parietal, or temporal cortex increasingly cerebral cortex. Instead, there are marked regional variations. differentiate and new areas emerge as one ascends the evolutionary This allowed the delineation of cortical areas, characterized by tree. In the human cortex, Brodmann defined 11 Hauptregionen a uniform cyto- or myeloarchitectonic pattern, and the defi- (regions), each of which was subdivided into a varying number nition of borders where the pattern changes. Among the first of Einzelfelder (areas). They were numbered consecutively from 1 who investigated the functional significance of these areas were to 52. However, there are two gaps in the sequence: areas 12, 13, Cécile and Oskar Vogt who also studied the cortex of non-human 14–16, and 48–51 were defined in lower mammals and non-human primates. In laboratory animals, microstructure can be directly primates, but they are missing in humans. This results in 43 areas correlated with function since upon completion of the functional in the human cortex. experiments (electrical stimulation of the cortex at that time) Brodmann’s map has become a “classic” in the field of neuro- the brains can be sectioned, stained for cell bodies or myelin biology. His ideas provided the basis for the concept of “localiza- sheaths, and stimulation sites compared with the architectonic tion” of function in the cerebral cortex – in sharp contrast to the pattern. Vogt and Vogt (1919) found that stimulation sites with “holistic” way of viewing brain functions (i.e., higher-level cog- comparable motor response properties lie within the same area. nitive abilities are functions of the entire brain and not of single However, across an architectonic border, the response properties cortical areas or modules). Despite many advances in neuroscience, change – first evidence that these areas are also functional enti- Brodmann’s nomenclature of cortical areas is still widely used to ties. Among several cytoarchitectonic maps of the human cortex designate functional regions in the cortex, e.g., area 4 for primary published in the first half of the twentieth century (Campbell, motor or area 17 for primary visual cortex. As to the functional 1905; Brodmann, 1909; von Economo and Koskinas, 1925; Bailey validity of Brodmann areas, it is important to note that cytoarchi- and von Bonin, 1951; Sarkissov et al., 1955), Brodmann’s map tectonic borders between these areas are also faithfully reflected became the most famous parcellation. In 1909 he published his on a neurochemical level, i.e., within the domain of synaptic findings in a comprehensive monograph entitled Vergleichende processing. Binding sites of “classical” neurotransmitters (e.g., Lokalisationslehre der Großhirnrinde (Treatise on Comparative acetylcholine, noradrenaline, glutamate, GABA), detected with Localization in the Cerebral Cortex; see also Annese, 2009; Zilles quantitative in vitro receptor autoradiography (Zilles et al., 2002), and Amunts, 2010). a technique developed in the second half of the twentieth century Frontiers in Human Neuroscience www.frontiersin.org February 2011 | Volume 5 | Article 19 | 1 Geyer et al. In vivo Brodmann mapping and many years after Brodmann’s death, exhibit marked laminar and/or flattening the cortex are available nowadays, e.g., FreeSurfer1, and regional variations in their cortical distribution patterns. It Caret2, or BrainVoyager3, the above problems with Brodmann’s has often been shown that borders defined by regional changes in map remain. these laminar binding patterns precisely match cytoarchitectonic On the other hand, functional imaging techniques, espe- “Brodmann borders” in adjacent sections stained for cell bodies, cially functional magnetic resonance imaging (fMRI), map the e.g., in the motor cortex (Geyer et al., 1996), premotor cortex cortex with ever-increasing spatial resolution, but they have so (Zilles et al., 1996), cingulate cortex (Palomero-Gallagher et al., far correlated activations only with macroanatomy (gyri and 2008), Broca’s region (Amunts et al., 2010), somatosensory cortex sulci). Invasive electrophysiology in experimental animals (e.g., (Geyer et al., 1997), parietal cortex (Zilles and Palomero-Gallagher, macaques), however, shows functional borders where micro- 2001; Scheperjans et al., 2005), auditory cortex (Morosan et al., anatomy changes (e.g., Luppino et al., 1991; Matelli et al., 1991). 2005), and visual cortex (Zilles et al., 2004; Eickhoff et al., 2008; Unfortunately, microanatomy is topographically variable across Zilles and Amunts, 2009). This means that not only does cellular brains (Rademacher et al., 1993; Geyer et al., 1996, 1999; Amunts microanatomy change at these “Brodmann borders,” but so too et al., 1999, 2000; Caspers et al., 2006) and hard to detect with does the entire organization of synaptic wiring and information MRI. Hence, structural–functional correlations based solely on processing. It is not surprising that Brodmann’s map has found macroanatomy are questionable and may account for at least some its way into the world of functional neuroimaging. Talairach and of the conflicting results functional imaging studies have provided Tournoux (1988, 1993) when establishing their stereotaxic ref- in the past. Talairach and Tournoux’s (1988, 1993) atlas is of lim- erence system for spatially normalizing imaging data, adopted ited value as well. The authors adopted Brodmann’s nomenclature Brodmann’s nomenclature for parcellating the cortex of their of areas, but their cortical maps are not based on microstructural standard brain in “Talairach Space.” data. In addition, the atlas indicates only the approximate posi- However, from today’s state-of-the-art neuroimaging perspec- tion of each area (borders between areas are not marked) and tive, several major problems arise when an investigator wants it ignores the problem of interindividual variability (only one to use the map as a structural guide to functional units in the brain is depicted). cerebral cortex. One way to overcome this dilemma is to generate proba- Firstly, more sensitive microstructural mapping techniques bilistic cytoarchitectonic maps in standard anatomical (e.g., developed since Brodmann’s time, e.g., neurofilament protein Montreal Neurological Institute, MNI) space (Roland and Zilles, immunohistochemistry (Baleydier et al., 1997) or in vitro trans- 1994). Cortical areas are defined cytoarchitectonically in post- mitter receptor autoradiography (Zilles et al., 2002) have revealed mortem brains, reconstructed in 3-D, and spatially normalized. functionally relevant subregions within many of the areas consid- Superimposing data from 10 brains gives a probabilistic description ered by Brodmann to be homogeneous. For example, area 19 is of each area’s spatial
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