Magnetic ROIs enable improved tractography accuracy through oriented prior
Maxime Chamberland1,2,3, Benoit Scherrer3, Sanjay Prabhu3, Joseph Madsen3, David Fortin4, Kevin Whittingstall2,5, Maxime Descoteaux1, and Simon K Warfield3

1Computer science, Université de Sherbrooke, Sherbrooke, QC, Canada, 2Nuclear Medicine and Radiobiology, Université de Sherbrooke, Sherbrooke, QC, Canada, 3Boston Children's Hospital, Harvard Medical School, Boston, MA, United States, 4Division of Neurosurgery and Neuro-Oncology, Université de Sherbrooke, Sherbrooke, QC, Canada, 5Department of Diagnostic Radiology, Université de Sherbrooke, Sherbrooke, QC, Canada

Synopsis

Streamline tractography algorithms infer connectivity by following directions which are maximally aligned at every voxel. This rule has even been the definition of the probability of connectivity, with the difference in current and next orientation being defined as uncertainty in connectivity. However, our experiments demonstrate that in regions where multiple fiber pathways interdigitate (e.g. temporal lobe), this heuristic is inadequate and does not necessarily reflect the underlying human brain architecture. Furthermore, we demonstrate that inference of connectivity can be improved by incorporating anatomical knowledge of the expected fiber orientation in regions where this information is known. We applied this heuristic through a new tractography region of interest (ROI) and demonstrate that it provides improved delineation of the expected anatomy.

Purpose

Connections of white matter are typically inferred from diffusion MRI using deterministic or probabilistic tractography algorithms1-4. These algorithms operate by taking as input orientation distributions functions, or a set of peaks, and by connecting adjacent voxels based on peaks that are maximally aligned1. However, not all fascicles are organized so that peaks along their course in the brain are maximally aligned. A perfect example of such caveat is the Meyer’s loop (ML), a highly curved fascicle known to exhibits a narrow turn, kissing/crossing regions, and changes in fascicle dispersion5. This fascicle is well understood from conventional Klinger dissection and histological analysis, and yet, the virtual reconstruction of the ML with tractography typically remains incomplete. Common methods encode our knowledge of the anatomy by solely using Boolean ROIs6 to include or exclude streamlines. We hypothesise that a new magnetic-ROI can help incorporate a priori information about the course of the pathway and lead to an improved delineation of the ML. The main goals of MAGNEtic Tractography (MAGNET) are thus to 1) increase the accuracy of tractography by selecting a specific direction based on a prior anatomical knowledge, and 2) reduce the total streamline calculation burden by avoiding an exponential search of all possibilities (i.e. computationally infeasible and inaccurate as it increases the amount of false positive4, 7).

Methods

The idea is to provide a preferential direction given by Vmagnet when a streamline enters a predefined magnetic-ROI. The most popular tracking equation1 is of the form: Vnext = argmink α(Vin ,Vk) (eq. 1), where Vnext is the next direction to propagate and α is the angle between the incoming direction Vin and the orientation of the kth peak Vk in the voxel. Instead, when tracking inside the new magnetic-ROI, we propose to follow the Vk that is most aligned with Vmagnet. The propagation equation becomes then: Vnext = { argmink α(Vmagnet,Vk) if inside the magnetic-ROI; eq. 1 otherwise }. If a voxel contains a single direction, the propagation naturally resumes with eq. 1. To measure the effect of our new evolution equation, MAGNET was applied on simulated data and on in vivo data obtained from 15 control subjects (10.2±3.1 years).

Synthetic dataset: A noiseless synthetic dataset consisting of 2 bundles crossing at 45° was generated using Phantomas8. A seed-ROI (Fig. 1a, purple box) and a magnetic-ROI (Fig. 1a, red box) were positioned in the peaks field. Streamline propagation was then qualitatively observed by activating MAGNET in real-time9.

Human datasets: Diffusion scans were performed using a multi-direction (90) and multi-b-value (range: 400-3000) scheme (TR/TE: 5700/89 ms, 1.7 × 1.7 × 2 mm3, CUSP9010) on a Siemens 3T Trio MRI. Multi-fiber model estimation was done using Diffusion Compartment Imaging (DCI)11, resulting in up to 3 main peaks per voxel. Tractography of the left optic radiation was performed using the following parameters: step size: 1 mm, θmax: 45°, maximum consecutive steps in the cortex: 5, min/max length: 60/200 mm. White matter/grey matter masks extracted from subject-specific anatomical T1-weighted images (1 mm isotropic) were used as tracking masks4. 3375 seeds were interactively9 placed anterolaterally to the left lateral geniculate nucleus (LGN)5, with initial seed direction oriented in the left direction (Fig 2a, "S"). An inclusion (AND) planar-ROI positioned at the midbody of the optic radiation and an exclusion (NOT) sagittal plane acted as filtering regions. To maximize the extent and coverage of the ML, magnetic-ROIs were then placed around the medial, anterior and lateral tip of the ML (Fig. 2a, b). These magnetic-ROIs favored the selection of DCI peaks that were oriented toward the visual cortex.

Results

Fig. 1 shows the effect of MAGNET on synthetic data. Activating the magnetic-ROI enabled specific selection of DCI peaks oriented toward the 45° pathway (Fig. 1c). Fig. 2 illustrates the magnetic-ROIs positioning for a single subject, as well as a conventional view of ML tractography. Fig.3 qualitatively shows that MAGNET successfully recovered a larger extent of ML for 15 subjects compared to traditional Boolean ROIs. Corresponding quantitative results are summarized in Tab.1. Finally, Fig. 4 shows an accurate comparison between MAGNET-based delineation of ML and histological drawing.

Conclusion

We showed that MAGNET can accurately reconstruct ML in all subjects. It effectively improved streamline coverage, and significantly reduced the ML-temporal pole and ML-inferior horn distances, crucial information for preoperative planning of temporal lobe surgery12. In future work, we plan to apply the magnetic operator inside automatically segmented anatomical structures (e.g. parcels). Our MAGNET technique is expected to enable unprecedented delineation of neural circuits not visible with conventional tracking algorithms.

Acknowledgements

The authors thank Chantal M. W. Tax for useful discussions.

Maxime Chamberland is supported by the Alexander Graham Bell Canada Graduate Scholarships-Doctoral Program (CGS-D3) from the Natural Sciences and Engineering Research Council of Canada (NSERC).

References

1Conturo et al. (1999) PNAS, 2Parker et al. (2003) JMRI, 3Sherbondy et al. (2008) J.Vis, 4Girard et al. (2014) Neuroimage, 5Martinez-Heras et al. (2015) PLoS ONE, 6Wakana et al. (2004) Radiology, 7Côté et al. (2013) Medical Image Analysis, 8Caruyer et al. (2014) ISMRM Milan, 9Chamberland et al. (2014) Frontiers in Neuroinformatics, 10Scherrer et al. (2012) PLoS ONE, 11Scherrer et al. (2015), Magnetic Resonance in Medicine, 12Tax et al. (2014) PLoS ONE.

Figures

Fig. 1: Synthetic reconstruction of 2 crossing bundles at 45° angle. a) Seed-ROI (4 × 2 × 2 mm3, purple) and magnetic-ROI (6 × 6 × 2 mm3, red, field orientation: left) overlaying simulated peaks. b) 1000 streamlines are initiated from the seed-ROI (magnetic-ROI: off). c) Streamlines entering the 45° pathway (magnetic-ROI: on).

Fig. 2: a, b) ROIs positioning. Purple box: seed region. Black lines: Boolean ROIs. Arrows indicate the direction of Vmagnet. c) Conventional Meyer’s loop tracking. A considerable amount of seeds exiting the LGN prefer to propagate towards the temporal pole (red) instead of entering the highly curved Meyer’s loop (green).

Fig. 3: MAGNET reconstruction of ML (green) shows visual improvements in volume coverage and anterior extent as opposed to conventional tractography using Boolean operators (blue). (Overlapping green streamlines may obscure underlying blue pathways due to an increased bundle density.) Visualization was done using the FiberNavigator9.

Fig. 4: Single subject (S5) MAGNET reconstruction of ML shows close agreement with histological studies (left). Ventricle segmentation (blue) was added to display the relationship between ML and the inferior horn. Colormap: T1-weighted image (S5). Anatomical drawing is courtesy of Dr. Patrick Roth.

Tab. 1: Quantitative evaluation of optic radiation tractography using conventional (BOOL) and MAGNET techniques. Significant differences are observed in streamline count, volume and relative distance measurements (3D). ML: Meyer’s loop. TP: Temporal pole. IH: Inferior horn. *: p < 0.005; **: p < 0.00005; ***: p < 0.000005.



Proc. Intl. Soc. Mag. Reson. Med. 24 (2016)
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