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. 2015 Aug 1;9:58-68.
doi: 10.1016/j.nicl.2015.07.005. eCollection 2015.

High-field Magnetic Resonance Imaging of the Human Temporal Lobe

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Free PMC article

High-field Magnetic Resonance Imaging of the Human Temporal Lobe

Luis M Colon-Perez et al. Neuroimage Clin. .
Free PMC article

Abstract

Background: Emerging high-field diffusion weighted MR imaging protocols, along with tractography, can elucidate microstructural changes associated with brain disease at the sub-millimeter image resolution. Epilepsy and other neurological disorders are accompanied by structural changes in the hippocampal formation and associated regions; however, these changes can be subtle and on a much smaller scale than the spatial resolution commonly obtained by current clinical magnetic resonance (MR) protocols in vivo.

Methods: We explored the possibility of studying the organization of fresh tissue with a 17.6 Tesla magnet using diffusion MR imaging and tractography. The mesoscale organization of the temporal lobe was estimated using a fresh unfixed specimen obtained from a subject who underwent anterior temporal lobectomy for medically refractory temporal lobe epilepsy (TLE). Following ex vivo imaging, the tissue was fixed, serial-sectioned, and stained for correlation with imaging.

Findings: We resolved tissue microstructural organizational features in the temporal lobe from diffusion MR imaging and tractography in fresh tissue.

Conclusions: Fresh ex vivo MR imaging, along with tractography, revealed complex intra-temporal structural variation corresponding to neuronal cell body layers, dendritic fields, and axonal projection systems evident histologically. This is the first study to describe in detail the human temporal lobe structural organization using high-field MR imaging and tractography. By preserving the 3-dimensional structures of the hippocampus and surrounding structures, specific changes in anatomy may inform us about the changes that occur in TLE in relation to the disease process and structural underpinnings in epilepsy-related memory dysfunction.

Keywords: DWI; Ex vivo brain imaging; High-field MRI; Mesoscale structure; Tractography.

Figures

Fig. 1
Fig. 1
Registration process from histology slides to MR image space. Landmarks in the MR image are identified and numbered (red numbers in image) and the same landmarks are identified in the original histology image. After non-linear registration the histology image can be overlaid on the MR image to qualitatively associate gray-scale landmarks with histology landmarks.
Fig. 2
Fig. 2
Clinical in vivo T2-weighted image. Higher intensity is observed in right hippocampus (left-side on image) and amygdala. The clinical diagnosis indicated secondary hippocampal edema.
Fig. 3
Fig. 3
Ex vivo-in vivo comparison of FA map with color reflecting the orientation of the largest maxima of the diffusion displacement probability. (A) Presurgical in vivo FA map at 1 mm isotropic spatial resolution reveals macro-scale white matter structures. The color sphere at the bottom right depicts the direction of largest displacement probability orientation. Blue, anterior–posterior; red, superior–inferior; and green, medial-lateral. (B) Enlargement of the white box of (A) illustrates the limited definition of internal features of the temporal lobe. (C) Down-sampled ex vivo FA map shows a slightly clearer delineation of the angular bundle, and some definition of the boundaries of the HC not visible in (B). In (B) and (C), the purple oval surround the hippocampus, the red circle surrounds the angular bundle and the blue oval surrounds the entorhinal cortex. (D) Cellular organization can be seen clearly in the high resolution ex vivo FA map. White matter structures including the angular bundle and the infrasubicular portion of the alveus are well delineated, as are multiple gray matter subdivisions (e.g. dentate granule cell layer, hippocampus proper, subiculum, and entorhinal cortex).
Fig. 4
Fig. 4
Anatomical compartments in the resected human temporal lobe according to Duvernoy (1988). (A) Temporal lobe sketch depicting important regions. (B) Average diffusivity map labeled with the subregions of A. The subregions are: 1—fuchsia = alveus, 2—green = CA3, 3—yellow = CA2, 4—red = CA1, 5—blue = subiculum, 6—mint = angular bundle, and 7—turquoise = entorhinal cortex. (C) Histological slide stained for neurofilaments (brown) and cell bodies (purple). (D) Fractional anisotropy (FA) map of ex vivo acquisition, arrows point two distinct pathways: one following inferior to CA1 and subiculum from alveus (red arrow in Parts D and E, gray in Part F) and second ventral to the first one following the perirhinal cortex surface (cortical region adjacent to entorhinal cortex, blue arrow in Parts D and E and white in Part F). (E) Average diffusivity map of ex vivo acquisition. The tracts dorsal to the hippocampus can be seen as two dark regions separated by a brighter area between them. (F) Orientation FA map, colors represent the direction of the largest maxima obtained by the diffusion displacement probability. The color sphere depicts the direction of largest displacement probability orientation: Blue, anterior–posterior; red, superior–inferior; and green, medial-lateral.
Fig. 5
Fig. 5
Microstructure of temporal lobe observed by histological sections. Grayscale image is the average diffusivity (AD) map acquired from the resected sample, displaying boundaries of figures (A–D) and gross anatomical features observed in the histological sections. In the AD image, the dentate granule cell body layer and inner molecular layer (A) correspond to a light band interior to a dark band that appears to correspond to the outer molecular layer. (B) At higher magnification (red box, (B)) regular microstructure begins to emerge, particularly the approximately parallel alignment exhibited by apical dendrites (APD, black arrows in Box C) of subicular pyramidal neurons. The turquoise Box (C) displays these apical dendrites oriented orthogonal to the dentate gyrus, and similar organization of the apical primary dendrites continues throughout CA1 and CA3. The green Box (D), which is the highest magnification of the histological sections, displays the apical dendrites organization parallel to each other in the subiculum. The diffusion measurements also show this organization (this figure).
Fig. 6
Fig. 6
Microstructural organization of the temporal lobe estimated by diffusion MRI overlayed onto fractional anisotropy maps. Grayscale on top left is the average diffusivity (AD) map displaying the boundaries of the regions displaying fiber orientations obtained by method of Wishart diffusion displacement probability maxima (A–C). (A) Red box displays the hippocampal regions, such as the subiculum and CA1, with largest maxima of water displacement in the direction to and from the dentate gyrus (parallel to red arrow) and the alveus. (B) Turquoise box displays the infra- subicular portion of the alveus traversing horizontally toward the entorhinal cortex. (C) Yellow box displays the angular bundle region with dominant orientation pointing anterior posterior.
Fig. 7
Fig. 7
Three-dimensional visualization of probabilistic and deterministic tractography results. (A) The perforant pathway streamlines compactly traverse through the angular bundle region, and distribute more broadly in the hippocampus and entorhinal cortex. (B) Probabilistic streamlines are obtained starting from a region of interest in the alveus and propagating to the rest of the image with no additional restrictions. The colors correspond to the number of streamlines passing through each voxel, yellow > red. Results were thresholded to display only voxels with 20 or more streamlines. (C–E) 3D streamlines traversing into the hippocampus, estimated by deterministic tractography. Yellow arrows point to streamlines of interest and the bottom left cube denote the orientation of the image. The streamlines in all images are in 3-dimensional space anterior to the slice shown in the background. (C) Coronal view of deterministic streamlines started in the alveus ROI and continued into the hippocampus. (D) Coronal view of streamlines passing through the subiculum and CA1 and extending into the dentate gyrus. (E) Oblique view of alveus (inferior to hippocampus) streamlines pointing to the entorhinal cortex and CA1 traversing inferior to the subiculum. (F) Oblique view of the alveus streamlines shown in (E) traversing inferior to the subiculum creating a sheet of streamlines rounding the inferior part of the hippocampus. In Parts E and F displays a dense, highly organized structure within the subiculum and CA1 region, resembling the general orientation of the apical dendrite organization observed with the immunohistochemistry analysis.

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