Identification of a distinct association fiber tract "IPS-FG" to connect the intraparietal sulcus areas and fusiform gyrus by white matter dissection and tractography

Abstract

The intraparietal sulcus (IPS) in the posterior parietal cortex (PPC) is well-known as an interface for sensorimotor integration in visually guided actions. However, our understanding of the human neural network between the IPS and the cortical visual areas has been devoid of anatomical specificity. We here identified a distinctive association fiber tract "IPS-FG" to connect the IPS areas and the fusiform gyrus (FG), a high-level visual region, by white matter dissection and tractography. The major fiber bundles of this tract appeared to arise from the medial bank of IPS, in the superior parietal lobule (SPL), and project to the FG on the ventral temporal cortex (VTC) in post-mortem brains. This tract courses vertically at the temporo-parieto-occipital (TPO) junction where several fiber tracts intersect to connect the dorsal-to-ventral cortical regions, including the vertical occipital fasciculus (VOF). We then analyzed the structural connectivity of this tract with diffusion-MRI (magnetic resonance imaging) tractography. The quantitative tractography analysis revealed the major streamlines of IPS-FG interconnect the posterior IPS areas (e.g., IP1, IPS1) with FG (e.g., TF, FFC, VVC, PHA2, PIT) on the Human Connectome Project multimodal parcellation atlas (HCP MMP 1.0). Since the fronto-parietal network, including the posterior IPS areas, is recruited by multiple cognitive demands, the IPS-FG could play a role in the visuomotor integration as well as the top-down modulation of various cognitive functions reciprocally.

Figure 1

Lateral view of IPS-FG in the left hemisphere. (A) The lateral view of left hemisphere after removal of the meninges and vessels, with representative anatomical landmarks. (B) The lateral view after dissection to expose the fiber bundles of IPS-FG. The frontoparietal and temporal opercula around the insula were removed to expose AF and VOF. (C,D) Further dissection after removal of VOF (C) and AF (D). (E–G) Isolation of IPS-FG in the left hemisphere. (H) Magnified image of the lateral occipital cortex in the left hemisphere. AF arcuate fasciculus, VOF vertical occipital fasciculus, ILF inferior longitudinal fasciculus, IFOF inferior fronto-occipital fasciculus, IPS intraparietal sulcus, POS parieto-occipital sulcus, TOS transverse occipital sulcus, PON pre-occipital notch, A anterior, P posterior, S superior.

Figure 2

Anatomical relationships among IPS-FG, AF, and VOF at the TPO junction. (A,B) Magnified images of the insula and temporo-parieto-occipital (TPO) junction to show the anatomical relationships among IPS-FG, AF and ILF/IFOF. (C,D) Tractography of the perisylvian language networks in the left hemisphere in the brain template (HCP1021). They consist of three subcomponents (long segment [AF long], anterior segment, and posterior segment [pAF]). (E) Lateral view shows the tractography of pAF (yellow), AF long (blue), and VOF (green). The white line shows the level of axial image in (F). (F) The axial view indicates the anatomical relationships among pAF (yellow), AF long (blue), and VOF (green) tractography in the brain template (HCP1021). (G) Axial view of the fiber orientation distribution functions (colored by orientation) overlaid on the T1-weighted image in the temporo-occipital lobe, in which the blue color indicate the voxels with vertically oriented fascicles. This area corresponds to the red rectangle region in (F). AF arcuate fasciculus, pAF posterior AF, VOF vertical occipital fasciculus, ILF inferior longitudinal fasciculus, IFOF inferior fronto-occipital fasciculus, A anterior, P posterior, S superior.

Figure 3

The cortical projections of IPS-FG on the dorsal and ventral cortex in dissection. (A,B) Caudal view of the left hemisphere after dissection of the cortex along the IPS and the TOS. (C) Posterolateral view of the brain after dissection to expose the fiber bundles of IPS-FG and VOF arising from IPS and TOS, respectively. “IPS-0, IPS-1, and V3A/B” indicate the anatomy-based visual filed maps. (D) Ventral temporal cortex (VTC) of the brain, showing the CoS (caudal, proper, and Rhinal segment), the OTS, the fusiform gyrus (orange), the inferior temporal gyrus (yellow), and the inferior occipital gyrus (green). (E,F) VTC of the brain after dissection of the cortex along the CoS to expose the fiber bundles of IPS-FG, running between CoS and OTS. IPS intraparietal sulcus, TOS transverse occipital sulcus, POS parieto-occipital sulcus, CoS collateral sulcus, OTS occipito-temporal sulcus, FG fusiform gyrus, ITG inferior temporal gyrus.

Figure 4

Reconstruction of IPS-FG tractography. (A) The ROIs of HCP MMP1.0 atlas, used for the fiber tracking of IPS-FG, were overlaid on the sagittal T1-weighted image. (B,C) Left and right lateral view of IPS-FG (red) with AF (blue) and VOF (green) tractography in the brain template (NTU-90), respectively. (D–F) Left and right lateral, and coronal view of the group-integrated tractography of IPS-FG overlaid on the sagittal T1-weighted image, respectively. (G) Lateral view of the IPS-FG (red), pAF (yellow), AF long (blue), and VOF (green) tractography in the brain template (HCP1021). The white line indicates the level of axial image in (H). (H) Axial view of tractography overlaid on the T1-weighted image to show the anatomical relationships among IPS-FG (red), pAF (yellow), AF long (blue), and VOF (green) in the temporo-occipital lobe. AF arcuate fasciculus, pAF posterior AF, VOF vertical occipital fasciculus, IPS intraparietal sulcus, AIP anterior intraparietal, VIP ventral intraparietal, MIP medial intraparietal, IP1, 2 intraparietal 1, 2, IPS1 intraparietal sulcus 1, LIPv lateral intraparietal ventral, LIPd lateral intraparietal dorsal, PHA2, 3 parahippocampal area 2, 3, V8 visual area 8, PIT posterior inferior temporal, FFC fusiform face complex, VVC ventral visual complex, VMV2, 3 ventro-medial visual areas 2, 3.

Figure 5

Streamline density maps, Connection index (CI), Connectogram, and Laterality index (LI). (A,B) Lateral view of streamline density maps for 60 subjects’ IPS-FG tractography, overlaid on T1-weighted image. (C) The tables indicate the Connection index (CI) for the tract numbers of each connection to link IPS areas and FG. Left; left hemisphere. Right; right hemisphere. Darker colors indicate the strength of connection. The data is average of healthy 60 subjects. (D) Connectogram representing bilateral connectivity patterns of IPS-FG, reflecting tract numbers of each connection. Circular color map represents the segmented brain regions that each streamline interconnects. The segmented arc and ribbon size represent the computed degrees of connectivity (the number of tracts) between segmented brain regions. The data is average of 60 subjects. (E) Graph indicates the laterality index (LI) for the tract numbers of IPS-FG in each subject (#1-60). The lowermost lane (red) is the average value of 60 subjects. The laterality index (left − right)/(left + right) shows the cerebral asymmetry. AIP anterior intraparietal, VIP ventral intraparietal, MIP medial intraparietal, IP1, IP2 intraparietal 1, 2, IPS1 intraparietal sulcus 1, LIPv lateral intraparietal ventral, LIPd lateral intraparietal dorsal, PHA2, 3 parahippocampal area 2, 3, V8 visual area 8, PIT posterior inferior temporal, FFC fusiform face complex, VVC ventral visual complex, VMV2, 3 ventro-medial visual areas 2, 3.