Comparative diffusion tractography of corticostriatal motor pathways reveals differences between humans and macaques - PubMed (original) (raw)

Comparative Study

. 2015 Apr 1;113(7):2164-72.

doi: 10.1152/jn.00569.2014. Epub 2015 Jan 14.

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Comparative Study

Comparative diffusion tractography of corticostriatal motor pathways reveals differences between humans and macaques

S F W Neggers et al. J Neurophysiol. 2015.

Abstract

The primate corticobasal ganglia circuits are understood to be segregated into parallel anatomically and functionally distinct loops. Anatomical and physiological studies in macaque monkeys are summarized as showing that an oculomotor loop begins with projections from the frontal eye fields (FEF) to the caudate nucleus, and a motor loop begins with projections from the primary motor cortex (M1) to the putamen. However, recent functional and structural neuroimaging studies of the human corticostriatal system report evidence inconsistent with this organization. To obtain conclusive evidence, we directly compared the pattern of connectivity between cortical motor areas and the striatum in humans and macaques in vivo using probabilistic diffusion tractography. In macaques we found that FEF is connected with the head of the caudate and anterior putamen, and M1 is connected with more posterior sections of the caudate and putamen, corroborating neuroanatomical tract tracing findings. However, in humans FEF and M1 are connected to largely overlapping portions of posterior putamen and only a small portion of the caudate. These results demonstrate that the corticobasal connectivity for the oculomotor and primary motor loop is not entirely segregated for primates at a macroscopic level and that the description of the anatomical connectivity of corticostriatal motor systems in humans does not parallel that of macaques, perhaps because of an expansion of prefrontal projections to striatum in humans.

Keywords: DTI; comparative anatomy; human; macaque; oculomotor.

Copyright © 2015 the American Physiological Society.

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Figures

Fig. 1.

Fig. 1.

Cortical seeds, striatal targets, waypoint masks, and corticostriatal streamlines in macaques and humans. Seed regions were defined as spheres with a 2-mm (macaques) or 4-mm (humans) radius. A: semitransparent 3-dimensional rendering from the T1-weighted image for macaques (top) and humans (bottom) with embedded caudate (orange) and putamen (yellow) and cortical seed regions: frontal eye fields (FEF) (green), M1 (red), and frontal pole (FP; blue). B: sagittal slices for macaques (top) and humans (bottom) with overlaid cortical seed regions (FEF, left columns), M1 (middle columns), and frontal pole (right columns), the group-averaged fiber streamlines from these regions (transparent corresponding colors), and the striatal regions caudate (orange) and putamen (yellow). Dashed lines show waypoint mask planes. Slice coordinates are in template space [Montreal Neurological Institute (MNI) space for humans, 112RM-SL space for macaques]. A, anterior; I, inferior; P, posterior; S, superior.

Fig. 2.

Fig. 2.

Classification maps of the probability a cortical seed was connected to the putamen and caudate nucleus, overlaid on 2-dimensional slices through the average normalized T1-weighted scan at the level of the striatum. The opacity of the overlay indicates the probability of connectivity (transparent voxels have a probability equal to 0; opaque voxels have a probability equal to 1).

Fig. 3.

Fig. 3.

Classification analysis of corticostriatal fibers in macaque and human. A: corticostriatal terminations in macaque (top) and human (bottom), pooled across hemispheres displayed on left-right (L-R) side views of caudate and putamen. Opaque colors indicate fiber termination zones based on group probability maps thresholded at P > 0.2. Arrows show orientation. B: distribution of corticostriatal connectivity and striatal volumes along the anterior-posterior (A-P) axis. Line charts show probability densities of total striatal volume along the A-P axis for macaque (dashed lines) and human (solid lines). The total area under the line charts represents the total striatal volume. Area charts show probability densities of corticostriatal connectivity along the A-P axis for macaque (vertically striped areas) and human (horizontally striped areas). For comparison across species and striatal regions, volume and fiber termination densities were normalized, so that the area under the line charts is equal to 1.

Fig. 4.

Fig. 4.

Connectivity index connectivity index (IC) as a function of group level probability threshold for data from M1 (red), FEF (green), and frontal pole (blue) from macaques (triangles) and humans (circles). This threshold reflects the number of subjects (humans or macaques) out of 7 for which a voxel was tagged at the single subject level that was needed to accept a voxel as being connected to the respective cortical seed at the group level. The size of each data point is proportional to the number of voxels on which the labeling index was computed. Data points for thresholds yielding connectivity <5% of the total striatal volume are not shown.

Fig. 5.

Fig. 5.

The classification analysis was repeated for 3 different minimum curvature thresholds used during probabilistic tractography: 120° allowing only relatively straight streamlines, 80° (the default value used in all the other analyses in this study), and 40° allowing very sharp bends in assessed streamlines. Top: outlines of the putamen and caudate as thin black lines projected on an axial slice through the striatum for humans and in colored lines with increasing thickness (reflecting decreasing minimal curvature) the outlines of the zones connected to the cortical seeds from left to right for the FEF (in green), M1 (in red), and frontal pole (in blue). Bottom: same data for macaques.

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