Human middle longitudinal fascicle: variations in patterns of anatomical connections - PubMed
Human middle longitudinal fascicle: variations in patterns of anatomical connections
N Makris et al. Brain Struct Funct. 2013 Jul.
Abstract
Based on high-resolution diffusion tensor magnetic resonance imaging (DTI) tractographic analyses in 39 healthy adult subjects, we derived patterns of connections and measures of volume and biophysical parameters, such as fractional anisotropy (FA) for the human middle longitudinal fascicle (MdLF). Compared to previous studies, we found that the cortical connections of the MdLF in humans appear to go beyond the superior temporal (STG) and angular (AG) gyri, extending to the temporal pole (TP), superior parietal lobule (SPL), supramarginal gyrus, precuneus and the occipital lobe (including the cuneus and lateral occipital areas). Importantly, the MdLF showed a striking lateralized pattern with predominant connections between the TP, STG and AG on the left and TP, STG and SPL on the right hemisphere. In light of the results of the present study, and of the known functional role of the cortical areas interconnected by the MdLF, we suggested that this fiber pathway might be related to language, high order auditory association, visuospatial and attention functions.
Figures

Method used to sample the seed for tractographic growing of the MdLF (green), which is shown in a lateral view of the left hemisphere of a representative subject. Three ROIs that included the entire white matter of the STG were drawn on the FA map as depicted in coronal images 1, 2 and 3 in the bottom row.

Delineation (2A) and differentiation (2B) of the middle longitudinal fascicle (MdLF). In 2A, the delineation of MdLF in the left hemisphere of a representative subject is shown in detail in five consecutive coronal sections (i-v) indicated on a parasagittal slice in the rostrocaudal dimension. In 2Ai, MdLF is present in the dorsal region (light green) of the temporal pole (TP). Further dorsally, 2Aii and 2Aiii, the MdLF is located within the superior temporal gyrus (STG), whereas in 2Aiv and 2Av, the MdLF is within the angular gyrus (AG). The lateral position of AG with respect to the intraparietal sulcus (inpars) guarantees the lateral location of AG in contrast to the medial location of the superior parietal lobule. In 2B, we show in a lateral view of the left hemisphere in a representative subject, all long association cortico-cortical fiber pathways in the hemisphere. Specifically, the MdLF, arcuate fascicle (AF), which courses adjacent and lateral to MdLF, the superior longitudinal fascicle II (SLF II) and superior longitudinal fascicle III (SLF III), extreme capsule/inferior frontooccipital fascicle (EmC/IFOF), inferior longitudinal fascicle (ILF), superior occipitofrontal fascicle (SFOF), uncinate fascicle (UF), and cingulum bundle (CB).

The predominant patterns of MdlF connections are shown in the left and right hemispheres of the same subject. The difference between left temporal pole (TP), superior temporal gyrus (STG) and angular gyrus (AG) pattern and the right TP, STG and superior parietal lobule (SPL) pattern is illustrated with clarity. It is noticeable how the MdLF is following a lower trajectory in the left hemisphere heading towards the angular gyrus, whereas on the right it pursues a higher route entering in the superior parietal lobule. A critical morphologically recognizable anatomical landmark using MRI for the differentiation of AG from SPL is the intraparietal sulcus (inpars), which constitutes a natural border of these two cortical regions, leaving AG on its lateral and SPL on its medial side.

Views of merged virtual tracts of all subjects. 4A. After merging the left and right MdLF tract from every subject, the resultant MdLF fiber bundle is shown. Panel “a” shows the frontal view, panel “b” shows the caudal view, panel “c” is the dorsal view, panel “d” is the ventral aspect and panels “e” and “f” show the lateral aspects of the right and left hemispheres respectively. 4B. Connections of all virtual fibers with cortical regions are illustrated. The MNI152 brain has been parcellated following the morphometric method of the Center for Morphometric Analysis at Massachusetts General Hospital (Caviness et al. 1996; Rademacher et al. 1992).

Frontal, lateral and inner views of merged virtual tracts of all subjects with cortical regions the tracts are connected to in the MNI152 standard coordinate space. In 5A, a frontal view shows all connections of MdLF observed in this study of 39 subjects (78 hemispheres) within the cerebral cortex. These are the temporal pole (TP), superior temporal gyrus (STG), supramarginal gyrus (SMG), superior parietal lobule (SPL), precuneus (PCN), temporo-occipital (T-O) and occipital lobe (OCC). Please note that in these cortical regions the angular gyrus should be included, which is a major connection of MdLF, however, is not visible in this frontal view, because it is covered by the SMG. The left and right temporal poles are magnified in the two sides of the figure to emphasize the prominent connection of MdLF within the dorsal region of the pole, which are readily visible in frontal views. In 5B, lateral and inner views show all cortical connections of MdLF observed in the left and right hemispheres. Although different in nature between right and left, the overall cortical regions involved are similar in both hemispheres and involve the temporal pole (TP), superior temporal gyrus (STG), supramarginal gyrus (SMG), superior parietal lobule (SPL), temporo-occipital region (T-O) and occipital lobe (OCC). Please note that in these cortical regions the precuneus (PCN; dark blue) should be included, which is not as visible in lateral or inner views, because covered by other structures. To allow visualization of more precise fiber-cortex relationships, the MNI152 brain has been parcellated following the morphometric method of the Center for Morphometric Analysis at Massachusetts General Hospital (Caviness et al. 1996; Rademacher et al. 1992).

Most frequently observed patterns of MdLF connections on the left and right hemispheres in 39 subjects (39 left and 39 right hemisphers) in the MNI152 standard coordinate space. To allow visualization of more precise fiber-cortex relationships, the MNI152 brain has been parcellated following the morphometric method of the Center for Morphometric Analysis at Massachusetts General Hospital (Caviness et al. 1996; Rademacher et al. 1992). Figure 6Ai-iv illustrates the most common pattern of MdLF in the left hemisphere (31%, i.e., 12 of 39 cases). In this pattern, the temporal pole (TP), superior temporal gyrus (STG) and angular gyrus (AG, BA 39), are connected by MdLF. In the bottom row, virtual fibers of MdLF (white) are clearly shown penetrating the AG and the dorsal part of TP. Figure 6Av-vii shows the second most common pattern of MdLF in the left hemisphere (13%, i.e., 5 of 39 cases). In this pattern, the TP, STG and superior parietal lobule (SPL, BA 7) are connected by MdLF. Virtual fibers of MdLF (white) are clearly shown penetrating the SPL and AG in a magnified detail. Figure 6Aviii-x depicts the third most common pattern of MdLF in the left hemisphere (8%, i.e., 3 of 39 cases). In this pattern, the TP, STG, supramarginal gyrus (SMG, BA 40) and AG (BA 39), are connected by MdLF. Virtual fibers of MdLF are shown penetrating clearly the SMG and AG in a magnified detail. Figure 6Bi-iv illustrates the most common pattern of MdLF in the right hemisphere (18%, i.e., 7 of 39 cases). In this pattern the TP, STG and SPL (BA 7), are connected by MdLF. In the bottom row, virtual fibers of MdLF are clearly shown penetrating the dorsal part of TP and the SPL in a magnified detail. Figure 6B v-vii shows the second most common pattern of MdLF in the right hemisphere (10%, i.e., 4 of 39 cases). Here, the TP, STG, AG (BA 39) and SPL (BA 7) are connected by MdLF. Virtual fibers of MdLF are clearly shown penetrating the AG and SPL in a magnified detail. Figure 6Bviii-x portrays an equally frequent pattern of MdLF in the right hemisphere as the one before (10%, i.e., 4 of 39 cases). Here, the TP, STG and AG (BA 39) are connected by MdLF. Virtual fibers of MdLF are clearly shown penetrating the AG in a magnified detail.

Most frequently observed patterns of MdLF connections on the left and right hemispheres in 39 subjects (39 left and 39 right hemisphers) in the MNI152 standard coordinate space. To allow visualization of more precise fiber-cortex relationships, the MNI152 brain has been parcellated following the morphometric method of the Center for Morphometric Analysis at Massachusetts General Hospital (Caviness et al. 1996; Rademacher et al. 1992). Figure 6Ai-iv illustrates the most common pattern of MdLF in the left hemisphere (31%, i.e., 12 of 39 cases). In this pattern, the temporal pole (TP), superior temporal gyrus (STG) and angular gyrus (AG, BA 39), are connected by MdLF. In the bottom row, virtual fibers of MdLF (white) are clearly shown penetrating the AG and the dorsal part of TP. Figure 6Av-vii shows the second most common pattern of MdLF in the left hemisphere (13%, i.e., 5 of 39 cases). In this pattern, the TP, STG and superior parietal lobule (SPL, BA 7) are connected by MdLF. Virtual fibers of MdLF (white) are clearly shown penetrating the SPL and AG in a magnified detail. Figure 6Aviii-x depicts the third most common pattern of MdLF in the left hemisphere (8%, i.e., 3 of 39 cases). In this pattern, the TP, STG, supramarginal gyrus (SMG, BA 40) and AG (BA 39), are connected by MdLF. Virtual fibers of MdLF are shown penetrating clearly the SMG and AG in a magnified detail. Figure 6Bi-iv illustrates the most common pattern of MdLF in the right hemisphere (18%, i.e., 7 of 39 cases). In this pattern the TP, STG and SPL (BA 7), are connected by MdLF. In the bottom row, virtual fibers of MdLF are clearly shown penetrating the dorsal part of TP and the SPL in a magnified detail. Figure 6B v-vii shows the second most common pattern of MdLF in the right hemisphere (10%, i.e., 4 of 39 cases). Here, the TP, STG, AG (BA 39) and SPL (BA 7) are connected by MdLF. Virtual fibers of MdLF are clearly shown penetrating the AG and SPL in a magnified detail. Figure 6Bviii-x portrays an equally frequent pattern of MdLF in the right hemisphere as the one before (10%, i.e., 4 of 39 cases). Here, the TP, STG and AG (BA 39) are connected by MdLF. Virtual fibers of MdLF are clearly shown penetrating the AG in a magnified detail.

Composite representations of the “seed” of the MdLF in 39 subjects in the Talairach space in left and right sagittal views. Three ROIs made up the seed in each hemisphere, namely an anterior ROI, a middle ROI and a posterior ROI. The Talairach coordinates (X = medio-lateral axis; Y = anterior-posterior axis; Z = vertical axis) of the center of mass of each ROI were as follows. Right anterior ROI: X = 52.2, Y = −8.3, Z = − 2.4; right middle ROI: X = 51.1, Y = −16.6, Z = 2.9; right posterior ROI = X = 51.2, Y = − 24.6, Z = 7.9. Left anterior ROI: X = −50.2, Y = −9.7, Z = −2.1; left middle ROI: X = − 49.6, Y = −18.1, Z = 3.0; left posterior ROI: X = −48.7, Y = −26.2, Z = 7.4.
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