A diffusion tensor MRI atlas of the postmortem rhesus macaque brain

Abstract

The rhesus macaque (Macaca mulatta) is the most widely used nonhuman primate for modeling the structure and function of the brain. Brain atlases, and particularly those based on magnetic resonance imaging (MRI), have become important tools for understanding normal brain structure, and for identifying structural abnormalities resulting from disease states, exposures, and/or aging. Diffusion tensor imaging (DTI)-based MRI brain atlases are widely used in both human and macaque brain imaging studies because of the unique contrasts, quantitative diffusion metrics, and diffusion tractography that they can provide. Previous MRI and DTI atlases of the rhesus brain have been limited by low contrast and/or low spatial resolution imaging. Here we present a microscopic resolution MRI/DTI atlas of the rhesus brain based on 10 postmortem brain specimens. The atlas includes both structural MRI and DTI image data, a detailed three-dimensional segmentation of 241 anatomic structures, diffusion tractography, cortical thickness estimates, and maps of anatomic variability among atlas specimens. This atlas incorporates many useful features from previous work, including anatomic label nomenclature and ontology, data orientation, and stereotaxic reference frame, and further extends prior analyses with the inclusion of high-resolution multi-contrast image data.

Keywords: Brain atlas; Diffusion tensor imaging; Macaca mulatta; Magnetic resonance imaging; Rhesus macaque; Tractography.

Figure 1

The eight different image contrasts included in the average atlas. For each contrast, a single axial slice through the basal ganglia is shown. GRE, gradient recalled echo; b=0, non-diffusion weighted image; DWI, isotropic diffusion weighted image; MD, mean diffusivity; RD, radial diffusivity; AD, axial diffusivity; FA, fractional anisotropy; FAC, directionally colored fractional anisotropy.

Figure 2

Comparison of single-subject vs. group average gradient echo anatomic images. A coronal slice through the hippocampus shows differences between a single-subject image (left half) and the group average image (right). Several anatomic structures are more apparent in the group average image (yellow arrowheads). In addition, some image artifacts are reduced in the group image due to averaging (red arrowheads). SLF II, superior longitudinal fasciculus II; Cl, claustrum; MD, mediodorsal thalamic nucleus; LGN, lateral geniculate nucleus; SNVL, substantia nigra compact part, ventrolateral division.

Figure 3

Demonstration of the atlas anatomic labels in two dimensions in the coronal plane. Five different coronal slices are presented as indicated by the slice diagram (top left). Adjacent slices are 7.5 mm apart. Each slice shows anatomic labels as red outlines (left half of images) and as semi-transparent color overlays (right half of images).

Figure 4

Demonstration of the atlas anatomic labels in three dimensions. (A) Lateral (top) and dorsal (bottom) views of the atlas brain surface. Major gyri and sulci are labeled for reference. (B) Lateral (top) and dorsal (bottom) views of atlas label surface renderings. Each different anatomic region is displayed with a different color surface. (C) Lateral (top) and dorsal (bottom) views of a surface rendering of the cerebral white matter tree (red). A semi-transparent rendering of the brain surface is included for reference. (D) Lateral (top) and posterior (bottom) views of surface renderings of five major subcortical structures: putamen (blue), caudate (yellow), hippocampus (green), external globus pallidus (teal), internal globus pallidus (orange). AG, angular gyrus; aspd, anterior supraprincipal dimple; ASPG, anterior superior parietal gyrus; cs, central sulcus; ecal, external calcarine sulcus; iar, inferior arcuate sulcus; IFG, inferior frontal gyrus; ios, inferior occipital sulcus; ipd, infraprincipal dimple; ips, intraparietal sulcus; lf, lateral fissure; lu, lunate sulcus; MFG, middle frontal gyrus; MG, marginal gyrus; MTG, middle temporal gyrus; OG, occipital gyrus; OTG, occipito-temporal gyrus; pos, parietooccipital sulcus; PrCG, precentral gyrus; PSPG, posterior superior parietal gyrus; sar, superior arcuate sulcus; SFG, superior frontal gyrus; spcd, superior precentral dimple; STG, superior temporal gyrus; sts, superior temporal sulcus; su, superior postcentral dimple; TPG, temporal polar gyrus.

Figure 5

Morphologic variation in the atlas. (A) A volume rendering of the mean positional difference (MPD) map generated from atlas diffeomorphic transforms. The color scale for the MPD map is shown in the center of the Figure. Relevant gyri and sulci are labeled for reference. (B) A volume rendered MPD map similar to (A), sliced axially through the arcuate sulcus. (C) Surface rendering of statistically significant voxel clusters for the voxel-based morphometry age correlation (false discovery rate adjusted, q<0.05). (D) t-statistic map for the voxel-based morphometry age correlation. The t-statistic color scale is shown in bottom right of Figure. Only regions that survived multiple comparison correction are colored. IFG, inferior frontal gyrus; MFG, middle frontal gyrus; iar, inferior arcuate sulcus; sar, superior arcuate sulcus.

Figure 6

Automated cortical thickness estimates for the average atlas generated using the DiReCT method. Thickness estimates are displayed as a colored surface rendering of the cortex. The color scale for cortical thickness estimates is shown in the center of the Figure. Relevant gyri and sulci are labeled for reference. (A) Lateral view. (B) Dorsal view. (C) Medial (midline) view. (D) Ventral view. CG, cingulate gyrus; Ins, insular cortex; lf, lateral fissure; OG, occipital gyrus; PrCG, precentral gyrus; sts, superior temporal sulcus; TPG, temporal polar gyrus.

Figure 7

Atlas tractography results. (A) Corpus callosum tractography divided into seven segments following the Witelson classification: genu (red), segment I (orange), segment II (yellow), segment III (green), segment IV (light blue), segment V (dark blue), splenium (purple). (B) Inferior (blue), middle (red), and superior cerebellar peduncles (green). (C) Cortical association pathways including: cingulum (red), middle longitudinal fasciculus (green), uncinate fasciculus (blue), and inferior longitudinal fasciculus (yellow).