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. 2020 Sep 7;56(9):452.
doi: 10.3390/medicina56090452.

Anatomical Characterization of the Human Structural Connectivity between the Pedunculopontine Nucleus and Globus Pallidus via Multi-Shell Multi-Tissue Tractography

Salvatore Bertino  1 , Gianpaolo Antonio Basile  1 , Giuseppe Anastasi  1 , Alessia Bramanti  2 , Bartolo Fonti  2 , Filippo Cavallaro  3 , Daniele Bruschetta  3 , Demetrio Milardi  1   3 , Alberto Cacciola  1
Affiliations

Anatomical Characterization of the Human Structural Connectivity between the Pedunculopontine Nucleus and Globus Pallidus via Multi-Shell Multi-Tissue Tractography

Salvatore Bertino et al. Medicina (Kaunas). .

Abstract

Background and objectives: The internal (GPi) and external segments (GPe) of the globus pallidus represent key nodes in the basal ganglia system. Connections to and from pallidal segments are topographically organized, delineating limbic, associative and sensorimotor territories. The topography of pallidal afferent and efferent connections with brainstem structures has been poorly investigated. In this study we sought to characterize in-vivo connections between the globus pallidus and the pedunculopontine nucleus (PPN) via diffusion tractography. Materials and Methods: We employed structural and diffusion data of 100 subjects from the Human Connectome Project repository in order to reconstruct the connections between the PPN and the globus pallidus, employing higher order tractography techniques. We assessed streamline count of the reconstructed bundles and investigated spatial relations between pallidal voxels connected to the PPN and pallidal limbic, associative and sensorimotor functional territories. Results: We successfully reconstructed pallidotegmental tracts for the GPi and GPe in all subjects. The number of streamlines connecting the PPN with the GPi was greater than the number of those joining it with the GPe. PPN maps within pallidal segments exhibited a distinctive spatial organization, being localized in the ventromedial portion of the GPi and in the ventral-anterior portion in the GPe. Regarding their spatial relations with tractography-derived maps of pallidal functional territories, the highest value of percentage overlap was noticed between PPN maps and the associative territory. Conclusions: We successfully reconstructed the anatomical course of the pallidotegmental pathways and comprehensively characterized their topographical arrangement within both pallidal segments. PPM maps were localized in the ventromedial aspect of the GPi, while they occupied the anterior pole and the most ventral portion of the GPe. A better understanding of the spatial and topographical arrangement of the pallidotegmental pathways may have pathophysiological and therapeutic implications in movement disorders.

Keywords: basal ganglia; brainstem; globus pallidus; pallidotegmental tract; pedunculopontine nucleus; structural connectivity; tractography.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Axial sections depicting masks of pallidal segments (A) and pedunculopontine nucleus (B) superimposed on the International Consortium for Brain Mapping (ICBM) template. Masks were labeled according to the subsequent color code: external globus pallidus (GPe) (blue), internal globus pallidus (GPi) (red), pedunculopontine nucleus (PPN) (yellow). Images are shown according to radiological convention.
Figure 2
Figure 2
Multiple axial slices showing the course of thresholded maximum probability maps (MPMs) of ipsilateral (A) and contralateral (B) tracts joining the PPN and GPi. Ipsilateral and contralateral MPMs have been superimposed on the ICBM template and displayed in the form of a lightbox, which shows the course of the average maps in a caudal-to-cranial direction. As shown by color bars, the voxel intensity is proportional to the number of subjects; thus, voxels characterized by lowest intensities overlapped in no more than 50 subjects, whereas voxels characterized by highest intensities overlapped across all subjects. Ipsilateral maps traverse the central tegmentum near the midline in the most caudal slices, travel in proximity to the red nucleus and, in the most cranial slices, enter the cerebral peduncle, finally reaching the GPi. Contralateral maps cross the midline at the mesencephalic decussation, as shown in the most caudal slices, and reach the contralateral GPi after entering the cerebral peduncle. Images are shown according to radiological convention.
Figure 3
Figure 3
Multiple axial slices showing the course of thresholded MPMs of tracts joining the PPN and GPe. MPMs have been superimposed on the ICBM template and displayed in the form of a lightbox, which shows the course of the average maps in a caudal-to-cranial direction. As shown by color bars, the voxel intensity is proportional to the number of subjects; thus, voxels characterized by lowest intensities overlapped in no more than 50 subjects, whereas voxels characterized by highest intensities overlapped in all subjects. Maps joining the PPN to the GPe ascend through the mesencephalic tegmentum in the most caudal slices and reach the GPe after entering the cerebral peduncle in the most cranial slices. Left and Right are reported according to radiological convention.
Figure 4
Figure 4
Spatial relations between PPN MPMs and the GPi. Axial slices of the ICBM template showing ipsilateral (A,B) and contralateral (C,D) PPN MPMs are superimposed as heatmaps on both the globus pallidus regions of interest (ROIs) and the pallidal limbic, sensorimotor and functional territories. Images are shown according to radiological conventions.
Figure 5
Figure 5
Spatial relations between PPN MPMs and the GPe. Axial slices of the ICBM template showing PPN MPMs superimposed on both the globus pallidus ROIs (A) and the pallidal limbic, associative and sensorimotor territories (B). Images are shown according to radiological conventions.
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