Cerebral Anatomical Variability

Even to describe a basic standard scheme of nomenclature for the cortical surface, we had to enter into the most difficult aspect of cerebral anatomy: the individual anatomical variability. This variability is a major point of consideration for anyone who wants to evaluate the quality of intersubject registration and normalization into a common space [18].

The degree of sulcal and gyral variability is partly related to timing of the genesis of the sulci during development [19]. The primary and secondary sulci appear early during brain development; they are constant and show a smaller variability than those that appear later during gestation. The earlier sulci are the interhemispheric fissure (8th gestational week), the Sylvian fissure and the callosal sulcus (14th gestational week), the parieto-occipital sulcus, and the Rolandic sulcus and the calcarine fissure (16th gestational week). The precentral, middle temporal, postcentral, intraparietal, superior frontal, and lateral occipital sulci develop between the 24th and 28th gestational weeks, together with the corresponding gyri. The latest sulci, which appear after the 28th gestational week, present the largest variability. For example, in the temporal lobe, the inferior temporal sulcus appears only during the 30th week of gestation and shows very large variability in the number of segments and duplications, making it difficult to identify as discussed earlier. During the final trimester of fetal life, tertiary gyri showing greater complexity develop, including the transverse temporal gyrus, the inferior temporal gyrus, the orbital gyri, and most especially the angular and supramarginal gyri, which, as discussed earlier, can be particularly difficult to define.

A thorough description of sulcal variability requires access to numerous brain specimens, and a very interesting approach has been taken by Ono, whose work we have already cited extensively. Ono made the only comprehensive atlas of the cerebral sulci, a first attempt to define sulcal variability statisically based on 25 autopsy brain specimens [15]. This author described the sulcal variability of the main constant sulci in terms of their incidence rate in each hemisphere; the number of interruptions, side branches, and connections; variations of shape, size, and dimensions; and the relationship to parenchymal structures. This descriptive work gives very valuable information but remains limited by the methodology used: the illustrations provided are photographs of the brain surfaces, and no information is given concerning the depth of the sulci. Furthermore, since it is a paper atlas, no 3D description is available. To overcome these limitations it is necessary to use a method that allows any brain to be described in a common fashion. Such a method has been developed by Jean Talairach [20-22], and variants of this method are described in the chapter entitled "Talairach Space as a Tool for Intersubject Standardization in the brain."

3.1 Sulcal Variability in Stereotactic Space

In the early 1970s, Jean Talairach finalized a methodology originally designed to allow neurosurgeons to practice functional surgery, especially thalamic surgery, in cases of serious Parkinsonian tremors (Fig. 4). This method was based on the identification of two structures: the anterior commissure (AC) and the posterior commissure (PC), to serve as landmarks defining a reference space into which any brain could be fitted. To define these landmarks, at a time when no tomographic imaging was available, Talairach combined a system of teleradiography, which maintained the true dimensions of the brain, together with ventriculography, which allowed the locations of the anterior and posterior commissures to be identified, to describe the relationship between these landmarks and individual anatomy. He did preliminary work on cadavers that led him to the conclusion that there was extensive variability in brain sizes but that the relationships of structures in the telencephalon to the AC, the PC and the AC-PC line were stable. He then defined a proportional grid localization system allowing him to describe anatomy in a statistical way, a very pioneering idea [20]. Within this system, it is possible to attribute to any structure in the brain three coordinates (x, y, z) and to refer to an atlas to assist in defining the structure (Fig. 4).

This proportional system makes it possible to describe the statistical anatomy of sulci, work first done by Talairach himself [20] providing an initial evaluation of the anatomical sulcal variability in his stereotactic space: approximately 20 mm for the left Rolandic sulcus. More modern estimates of sulcal variability in this stereotactic space, based on tomographic magnetic resonance images, remain large, around 12 to 20 mm [10]. A major point to emphasize is that a crucial component of this variation is the stereotactic space itself. Structures near the AC or PC exhibit smaller variations than structures at the outer limit of the cortex [23]. These two points are illustrated in Fig. 5. This means that accuracy of localization in the stereotactic space remains limited to around 1 to 2 cm, a result both of intrinsic sulcal and gyral variability and of bias in the normalization procedure. This study used linear deformations to enter into the common space. New algorithms allowing a more precise alignment of one brain to the target brain have been developed, leading to a reduction of intersubject sulcal variability in the stereotactic space [18,24,25]. These have been validated using anatomical landmarks such as sulci, to demonstrate their impact on anatomical variability (see Fig. 6). This is an example of how anatomy can be used within the framework of brain averaging, and also a demonstration that the residual sulcal variability after normalization into the stereotactic space can be reduced by tools allowing better brain registration.

The major point of the Talairach system is that it allows a statistical description of anatomy, a topic that has been rediscovered with the advent of anatomical magnetic resonance imaging (aMRI). A nice example can be found in the work of Paus [17] using midbrain sagittal slices of normal volunteers. In a group of 247 subjects, he manually drew in each subject the calloso-marginal sulcus (also called the cingulate sulcus) and the paracingulate sulcus when it was present. He then normalized these regions of interest (ROIs) into the Talairach space. This allowed him to generate probabilistic maps of these sulci, one per hemisphere, as shown in Fig. 7. He discovered that there was a striking asymmetry in the prominence of the paracingulate sulcus favoring the left hemisphere, which he related to the participation of the anterior part of the left cingulate cortex during language tasks. Another study in stereotactic space showed a leftward asymmetry of Heschl's gyrus, which is the location of the primary auditory area in each hemisphere [26], and related this asymmetry to the left temporal cortex specialization for language in right-handers. These works are the beginning of a new era for anatomy: probabilistic anatomical maps elaborated with large population of subjects. These are the core or what seems the bright future of anatomy.

3.2 Brain Asymmetries

An important type of variability within the brain relates to the differences between the two hemispheres that seem symmetrical at first glance. Indeed, the brain was generally believed to be anatomically symmetrical until 1968; when Geschwind first described a macroscopic asymmetry in the temporal lobe, namely in the planum temporale [27]. This region lies just

FIGURE 4 Talairach coordinate system. Individual volumes are first reoriented and translated into a common frame of reference based on two specific cerebral structures: the anterior and the posterior commissures (AC and PC, respectively). This system was built on the observation that the positions of these subcortical structures were relatively invariant between subjects. A bicommissural frame of reference is then formed by three planes orthogonal to the interhemispheric plane of the brain: a horizontal one passing through the AP and the PC (the AC-PC plane) and two vertical ones passing respectively through the AC and the PC (the ACV and the PCV planes). Once reoriented, the subject's brain is rescaled in that orientation along the three principal axes to adjust its global size and shape to that of a specific brain (generally referred to as the template) in this frame of reference. Finally, cerebral structures are represented by three coordinates (x, y, z) indicating their position in the Talairach system. See also Plate 61.

FIGURE 5 Sulci of the internal surface of the brain individually drawn in six postmortem human brains (PAOC, parietoccipital sulcus; CALC, calcarine sulcus; CALL, callosal suclus; CING, cingulate sulcus; adapted from Thompson et al. [23]). This figure illustrates the directional bias in sulcal variability, in the horizontal and vertical directions, given in millimeters in the left hemisphere (after transformation into sterotactic space). The profile of variability changes with distance from the posterior commissure, ranging from 8-10 mm internally to 17-19 mm at the exterior cerebral surface. Moreover, the spatial variability is not isotropic, since the variability of the occipital sulcus is greater in the vertical direction, while that of the paralimbic sulcus is larger in the horizontal direction. This is partly due to developmental effects, but is also related to the type of spatial transformation model used for normalization. For example, the calcarine sulcus is bounded anteriorly by the PC point and posteriorly by the posterior tip of the brain, constraining its variability in the anteroposterior direction. See also Plate 62. Reprinted with permission from P. M. Thompson, C. Schwartz, R. T. Lin, A. A. Khan, and A. W. Toga, Three-dimensional statistical analysis of sulcal variability in the human brain. J. Neurosci. Vol. 16, pp. 4261-4274, 1996.

FIGURE 5 Sulci of the internal surface of the brain individually drawn in six postmortem human brains (PAOC, parietoccipital sulcus; CALC, calcarine sulcus; CALL, callosal suclus; CING, cingulate sulcus; adapted from Thompson et al. [23]). This figure illustrates the directional bias in sulcal variability, in the horizontal and vertical directions, given in millimeters in the left hemisphere (after transformation into sterotactic space). The profile of variability changes with distance from the posterior commissure, ranging from 8-10 mm internally to 17-19 mm at the exterior cerebral surface. Moreover, the spatial variability is not isotropic, since the variability of the occipital sulcus is greater in the vertical direction, while that of the paralimbic sulcus is larger in the horizontal direction. This is partly due to developmental effects, but is also related to the type of spatial transformation model used for normalization. For example, the calcarine sulcus is bounded anteriorly by the PC point and posteriorly by the posterior tip of the brain, constraining its variability in the anteroposterior direction. See also Plate 62. Reprinted with permission from P. M. Thompson, C. Schwartz, R. T. Lin, A. A. Khan, and A. W. Toga, Three-dimensional statistical analysis of sulcal variability in the human brain. J. Neurosci. Vol. 16, pp. 4261-4274, 1996.

behind Heschl's gyrus, which corresponds to the primary auditory area. Eighteen years later, the advent of aMRI allowed Steinmetz to develop a method to measure the planum temporale surface in normal volunteers. He first confirmed the existence of a leftward asymmetry in right-handers [28] and then demonstrated that this asymmetry was diminished in lefthanders [29]. These results argue, as was suggested by Geschwind, for a role of this region in the left hemisphere dominance for language, making the study of anatomical asymmetry of great interest. These asymmetries might even reflect a particular organization for language in an individual.

For example, the absence of a clear asymmetry in a subject might predict ambilaterality in terms of hemispheric organization for language.

Some other regions show anatomical asymmetries, and they are all parts of the language network: Broca's area [30] and, as already mentioned, the paracingulate sulcus ([17], Fig. 7) and the left Heschl's gyrus [26]. The corpus callosum, which is very likely to reflect interhemispheric transfer of information, also shows important anatomical variability that seems to be related with gender differences, although this point is still under debate [31].

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