Spatial organization of occipital white matter tracts in the common marmoset

Abstract

The primate brain contains a large number of interconnected visual areas, whose spatial organization and intracortical projections show a high level of conservation across species. One fiber pathway of recent interest is the vertical occipital fasciculus (VOF), which is thought to support communication between dorsal and ventral visual areas in the occipital lobe. A recent comparative diffusion MRI (dMRI) study reported that the VOF in the macaque brain bears a similar topology to that of the human, running superficial and roughly perpendicular to the optic radiation. The present study reports a comparative investigation of the VOF in the common marmoset, a small New World monkey whose lissencephalic brain is approximately tenfold smaller than the macaque and 150-fold smaller than the human. High-resolution ex vivo dMRI of two marmoset brains revealed an occipital white matter structure that closely resembles that of the larger primate species, with one notable difference. Namely, unlike in the macaque and the human, the VOF in the marmoset is spatially fused with other, more anterior vertical tracts, extending anteriorly between the parietal and temporal cortices. We compare several aspects of this continuous structure, which we term the VOF complex (VOF +), and neighboring fasciculi to those of macaques and humans. We hypothesize that the essential topology of the VOF+ is a conserved feature of the posterior cortex in anthropoid primates, with a clearer fragmentation into multiple named fasciculi in larger, more gyrified brains.

Keywords: Comparative anatomy; Diffusion MRI; Marmoset; Vertical occipital fasciculus; Visual cortex; White matter.

Figure 1.. Major occipital white matter tracts in marmoset are visible in DEC maps from diffusion MRI data.

The color schema represents the principal diffusion direction in each voxel (red, left-right; green, anterior-posterior; blue, superior-inferior) in representative coronal (a-c; posterior to anterior) or axial slices (d-e; inferior to superior) of a marmoset brain (marmoset1). Scale bars in each panel indicate 5 mm. Yellow lines show the slice position presented in the other orthogonal slices. OR: optic radiation, Forceps: forceps major, VOF+: Vertical occipital fasciculus complex, Cal: Calcarine sulcus, LGN: Lateral geniculate nucleus.

Figure 2.. Tractography of three major occipital white matter tracts in marmoset, macaque and humans.

Axial (top panels) and sagittal view (bottom panels) of tractography overlaid on anatomical images in representative subjects for each of species. In all species, we identified the optic radiation (green), forceps major (dark yellow), and VOF/VOF+ (blue). Spatial scales differ across species and are indicated by the white bar in each panel.

Figure 3.. FA comparison across species along major occipital white matter tracts.

A. Left panel: Tract positions were (white dotted line) overlaid on axial slices of DEC maps of marmoset (top panel, marmoset1), macaque (middle panel) and human data (bottom panel, human1). Right panel: FA maps of the same axial slices as the left column. Color coding of FA maps is depicted in color bars on the right. The scale bar in each plot indicates 5 mm. B. Mean of FA value along each tract in marmoset (top panel), macaque (middle panel) and human data (bottom panel; see Methods section for the detail). Bars represent averaged FA across hemispheres, while red circles depict FA of tracts in individual hemispheres.

Figure 4.. Putative cortical endpoints of marmoset VOF+ streamlines.

A. Normalized VOF+ streamline endpoint density (averaged across 4 hemispheres) represented over the cortical surface model of the marmoset brain atlas with cortical parcellations defined by comparisons between MRI and histology data (Hashikawa et al., 2015; Woodward et al., 2018). Top panel: Dorsal endpoint of marmoset VOF+. Bottom panel: Ventral endpoint of marmoset VOF+. The intensity of colors indicates normalized VOF+ streamline endpoint counts in each vertex (red, top panel; blue, bottom panel). B. VOF+ endpoints coverage of each cortical area for dorsal (top panel) and ventral endpoint (bottom panel), respectively. The vertical axis indicates proportions of voxels in each area which have normalized VOF+ streamline endpoint counts larger than 0.5. See Methods for further details in this analysis.

Figure 5.. Comparison between marmoset VOF+ with pAF and VOF of macaque and human.

A. Top left panel: Marmoset VOF+ subdivided into anterior and posterior subcomponents. Red streamlines are VOF+ subcomponent with dorsal endpoints near posterior parietal cortex. Blue streamlines are the other VOF+ subcomponent with dorsal endpoints near dorsal occipital cortex. Middle and bottom left panels: Macaque (middle) and human (bottom) pAF and VOF. Red streamlines are pAF and blue streamlines are VOF. Right panels: The positions of each fasciculus or subcomponent were shown as red or blue contours and are overlaid on an axial slice of the structural image. Unlike those in macaque and human, two VOF+ subcomponents in marmoset (top right panel) did not exhibit a clear separation. The scale bars indicate 5 mm. B. The proportion of voxels in which two fasciculi overlap in marmoset, macaque and human. While this plot is based on single subject for each species, we note that results are highly consistent in another marmoset brain and other human datasets.