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Meta-Analysis
. 2010 May 5;30(18):6409-21.
doi: 10.1523/JNEUROSCI.5664-09.2010.

Anatomical and Functional Connectivity of Cytoarchitectonic Areas Within the Human Parietal Operculum

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Free PMC article
Meta-Analysis

Anatomical and Functional Connectivity of Cytoarchitectonic Areas Within the Human Parietal Operculum

Simon B Eickhoff et al. J Neurosci. .
Free PMC article

Abstract

In monkeys, the somatosensory cortex on the parietal operculum can be differentiated into several distinct cortical fields. Potential human homologues for these areas have already been defined by cytoarchitectonic mapping and functional imaging experiments. Differences between the two most widely studied areas [operculum parietale (OP) 1 and OP 4] within this region particularly pertain to their connection with either the perceptive parietal network or the frontal motor areas. In the present study, we investigated differences in anatomical connection patterns probed by probabilistic tractography on diffusion tensor imaging data. Functional connectivity was then mapped by coordinate-based meta-analysis of imaging studies. Comparison between these two aspects of connectivity showed a good congruency and hence converging evidence for an involvement of these areas in matching brain networks. There were, however, also several instances in which anatomical and functional connectivity diverged, underlining the independence of these measures and the need for multimodal characterization of brain connectivity. The connectivity analyses performed showed that the two largest areas within the human parietal operculum region display considerable differences in their connectivity to frontoparietal brain regions. In particular, relative to OP 1, area OP 4 is more closely integrated with areas responsible for basic sensorimotor processing and action control, while OP 1 is more closely connected to the parietal networks for higher order somatosensory processing. These results are largely congruent with data on nonhuman primates. Differences between anatomical and functional connectivity as well as between species, however, highlight the need for an integrative view on connectivity, including comparison and cross-validation of results from different approaches.

Figures

Figure 1.
Figure 1.
A, Organization of cortical areas in the lateral sulcus of nonhuman primates [adopted and summarized from Disbrow et al. (2003) and Krubitzer et al. (1995)]. It should be noted that inconsistent evidence for further somatosensory areas in this region has been discussed and that a subdivision of VS into two separate areas, VSr (rostral) and VSc (caudal), has been proposed (Coq et al., 2004). B, Anatomical organization of the human parietal operculum. Four distinct cytoarchitectonic areas (termed OP 1–4) have been delineated in this region using quantitative histological analysis. Following 3D reconstruction of the cytoarchitectonically analyzed postmortem brains and spatial normalization of these areas into the reference space of the MNI, probabilistic maps for the areas were computed and subsequently combined into an MPM. This anatomical MPM indicates the most likely area at each voxel of the reference space and is shown here in a ventral view on a surface rendering of the MNI single-subject template. The temporal lobes have been removed to obtain an unobstructed view onto the parietal operculum, where the different colors correspond to OP 1–4 as marked. Based on topography and somatotopic organization, OP 4 should correspond to primate area PV, OP 1 to area S2, and OP 3 to area VS. Finally, OP 2 is the homologue of the parietoinsular vestibular cortex in nonhuman primates. Bars in the histological images denote 1 mm. C, Three-dimensional surface rendering of the MNI single-subject template after removal of the temporal lobe. The position of areas OP 1 and OP 4 as defined by their MPM representation is indicated on this view in red and green, respectively. In contrast to panel B, which gives a view directly facing the parietal operculum, the tilted view used in this panel provides an overview on the extent of OP 1 and OP 4 on the free surface. Together with B, it can be seen that OP 4 encroaches the free surface of the subcentral gyrus while covering about two-thirds of the mediolateral width of the parietal operculum. Area OP 1, on the other hand, barely reaches the free surface but covers about three-fourths of the mediolateral width of the parietal operculum.
Figure 2.
Figure 2.
Top and middle panels, Seeds and targets were defined by representations of the respective cytoarchitectonic areas in an MPM of all histologically defined regions. This MPM is shown in the background of the figures in the top row. Different shades of gray denote the different cytoarchitectonic areas. For the sake of display clarity, however, these areas are not individually labeled in these figures. In the displayed example, the seed region was defined by the anatomical location of area OP 4, which is indicated in green. The volume of interest defining this seed, i.e., the location of area OP 4, is then transformed into single-subject diffusion space for probabilistic tractography. Quantitative analysis was then based on the sample count obtained from these analyses, i.e., the number of probabilistic traces originating from the seed (OP 1 or OP 4) reaching a particular target (cf. Table 1). For visualization, the ensuing tracts were also back-projected into the MNI space and averaged to represent the mean pathways. In the figures on the top and middle right, the color scale from red to yellow indicates the probability that the respective tract passes through the respective voxel as obtained from probabilistic tractography. MNI space refers to the reference space defined by the Montreal Neurological Institute for the definition of stereotaxic coordinates (Collins et al., 1994; Evans et al., 1992), which currently represents the most widely used standard for multisubject analysis of neuroimaging data. Bottom panel, Surface rendering of the target regions covering the frontal and parietal cortices displayed on a surface rendering of the MNI template. Each of these cytoarchitectonically defined targets is transformed into the single-subject diffusion space in the same manner as illustrated above for a seed region. An overview on the acronyms used to label the different regions as well as further information on these and their cytoarchitectonic correlates is given in Table 1.
Figure 3.
Figure 3.
Examples of white matter fiber pathways as obtained from probabilistic tractography for OP 1 (A) and OP 4 (B) reconstructed in 3D. The data shown here illustrate the tracts connecting OP 1 and OP 4, respectively, with exemplary target regions (cf. Table 1) and hence reveal the pathways taken by the fiber tracts connecting the seeds and targets. The absolute strength of these connections, in turn, are summarized in Figure 4. All examples are displayed on the transparent MNI single-subject template. (d: dorsal, v: ventral, l: left, ri: right, ro: rostral, c: caudal). The color scales ranging from dark to light blue and from red to yellow, respectively, denote the probability that the particular tract runs through a given voxel. Light blue or yellow indicates those locations in the white matter where the respective pathways are very likely to be found. Dark blue or red, on the other hand, indicate less likely positions of the connecting fibers.
Figure 4.
Figure 4.
Mean connection strength (across subjects) between human parietal operculum (OP 1 and OP 4) and 12 different target regions assessed in the current study. Quantitative tractography was based on the sample count obtained when performing probabilistic tractography from the seed regions (OP 1 or OP 4) to the different targets (cf. Table 1) after these were transformed into the individual diffusion spaces of each subject. The connection probabilities obtained by this probabilistic tractography were normalized by dividing by the total connection probability of each seed and rescaled by multiplying by the mean total probability across all seeds and targets. Finally, connection densities were divided by the size of the target VOIs, computed on an individual basis, and again rescaled by the mean size of all targets to provide normalized connection strengths. The circles indicate the mean connection strength of each target with the entire parietal operculum, i.e., areas OP 1 and OP 4. The bars denote the 95% confidence intervals on these connection strengths.
Figure 5.
Figure 5.
The statistical analysis of the anatomical connectivity data revealed a significant interaction between “seed” and “target” (F = 7.83; p < 0.001), indicating a difference in the patterns of frontoparietal connectivity between OP 1 and OP 4. Here, the anatomical connectivity of OP 1 and OP 4 to the different target regions is analyzed, resolving this “seed” × “target” interaction. In the left panel, the normalized connection strengths to all targets are displayed for both areas. The dark gray bars indicate the anatomical connectivity of OP 1, the medium gray bars indicate that of OP 4, and the error bars denote the SE. The right panel shows the difference between OP 1 and OP 4 connectivity. Significant (p < 0.05, corrected) differences between these two seeds with respect to the anatomical connectivity to a particular target are indicated by gray scale bars (dark gray bars indicate a significantly higher connectivity of OP 1 to this target, and medium gray bars indicate a significantly higher connectivity of OP 4) and asterisks. Light gray bars denote targets for which no significant difference in the anatomical connectivity with OP 1 and OP 4, respectively, were found.
Figure 6.
Figure 6.
A, Functional connectivity of the human parietal operculum as delineated by the significant (p < 0.05, corrected) coactivation pattern obtained in a meta-analysis of 245 neuroimaging studies activating either OP 1 or OP 4. The color denotes the significance of the respective results. That is, while the presence of color indicates voxels that are significantly coactivated with the seed region, the particular color indicates the strength of this effect (z-score of the statistical analysis). B, Strength of functional connectivity between the human parietal operculum and the different anatomically defined targets assessed in this study (compare Fig. 4) as defined by the volume fraction of the targets' MPM representations that were significantly coactivated with OP 1 or OP 4. The labels in this graph confirm to the acronyms summarized for reference in Table 1. C, Comparison of the functional and anatomical connectivity of the human parietal operculum, i.e., OP 1 and OP 4 combined. The data used for this diagram correspond to the results shown in Figures 4 and 6B. However, to allow a direct comparison, the connection strengths displayed in Figures 4 and 6B were rescaled to unit total connectivity, accounting for the different scaling of the data obtained from the analysis of functional and anatomical connectivity. Again, labels in this graph confirm to the acronyms explained in Table 1.
Figure 7.
Figure 7.
A, Functional connectivity of area OP 1 as delineated by the significant coactivation pattern obtained in a meta-analysis of the 80 studies activating only this area. As in Figure 6, the color scale ranging from deep red to white-yellow indicates the strength of the effects (z-score of the statistical analysis; all indicated voxels were significantly coactivated at p < 0.05, cluster level corrected). B, Functional connectivity of area OP 4 as delineated by the significant coactivation pattern obtained in a meta-analysis of the 61 studies activating only this area. Again, the color scale indicates the statistical effect size. C, Regions showing significant difference in functional connectivity between areas OP 1 and OP 4. Red indicates those voxels that were significantly more often coactivated with OP 1 as compared with OP 4; voxels shown in green denote those regions that showed significantly higher probabilities of coactivating with OP 4 than with OP 1. All data shown at p < 0.05, corrected.
Figure 8.
Figure 8.
A, Comparison of the differences between OP 1 and OP 4 in terms of their anatomical (as assessed by probabilistic tractography) and functional (as assessed by meta-analysis of neuroimaging data) connectivity to the assessed frontoparietal targets. Each target is represented by a data point indicated by the position of its acronym on a two-dimensional coordinate grid. The x-coordinate of this point indicates the difference in functional connectivity (quantified by coactivated volume fraction) between this target and OP 1 on one hand and OP 4 on the other. Precisely, the x-value of target acronym's position is equivalent to the strength of functional connectivity between this target and OP 1 minus the strength of functional connectivity between this target and OP 4. The y-coordinate indicates the difference in anatomical connectivity (quantified by normalized connection strength). That is, the y-value of target acronym's position is equivalent to the strength of anatomical connectivity from OP 1 and this target minus the strength of anatomical connectivity from OP 4 and this target. It may be argued that one or both of these measures may be confounded by the physical distance between seed and target. Hence, differences in anatomical and functional connectivity were also plotted against the difference between OP 1 and OP 4 in their physical distance (quantified by the mean Euclidean distance across seed voxels to the nearest target voxel) to the respective target. B and C, The comparison between anatomical connectivity and physical (Euclidean) distance is shown in B, and the comparison between functional connectivity and physical distance is shown in C. It can be seen that differences between OP 1 and OP 4 in terms of functional and anatomical connectivity are significantly correlated to each other but not to physical distances to the targets.
Figure 9.
Figure 9.
Behavioral domain profiles for all those experiments that feature at least one activation in OP 1 and OP 4, respectively. BrainMap counts (light gray histograms) represent the proportion of experiments in BrainMap that relate to the particular BD category. Dark gray and medium gray histograms represent the proportion of experiments featuring an activation in OP 1 and OP 4, respectively, that belong to the particular BD. All histograms were significantly different from each other with respect to overall shape. Asterisks denote significant (p < 0.05) differences in the individual comparisons.

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