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Reconstruction of the Human Visual System Based on DTI Fiber Tracking

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Reconstruction of the Human Visual System Based on DTI Fiber Tracking JOURNAL OF MAGNETIC RESONANCE IMAGING 26:886–893 (2007) Original Research Reconstruction of the Human Visual System Based on DTI Fiber Tracking Philipp Staempfli, PhD,1,2* Anna Rienmueller, MD,1 Carolin Reischauer, MSc,1 Anton Valavanis, MD,2 Peter Boesiger, PhD,1 and Spyridon Kollias, MD2 has been proposed so far (for review articles, see Refs. 6 Purpose: To apply and to evaluate the newly developed and 7). Despite the promising applications of DTI fiber advanced fast marching algorithm (aFM) in vivo by recon- structing the human visual pathway, which is character- tracking in brain research and clinical studies, this ized by areas of extensive fiber crossing and branching, i.e., technique is still constricted by several limitations. A the optic chiasm and the lateral geniculate nucleus (LGN). severe drawback is the tensor’s voxel-averaged nature, i.e., the principal eigenvector does not necessarily cor- Materials and Methods: Diffusion tensor images were ac- quired in 10 healthy volunteers. Due to the proximity to respond to the main fiber direction, particularly when bony structures and air-filled spaces of the optic chiasm, a bundles intersect, branch, or merge. For whole-brain high sensitivity encoding (SENSE) reduction factor was ap- DTI fiber tracking, the voxel size of the data that can be plied to reduce image distortions in this area. To recon- achieved in a clinically feasible acquisition time is ap- struct the visual system, three different seed areas were proximately 1.5 mm3. This is orders of magnitudes chosen separately. The results obtained by the aFM track- larger than the diameter of a single axon, which lies in ing algorithm were compared and validated with known the range of a few microns. Therefore, only major fiber anatomy. bundles can be resolved, and it is not possible to trace Results: The visual system could be reconstructed repro- the course of single axons with DTI. But even when ducibly in all subjects and the reconstructed fiber path- main fiber systems are investigated, trajectories may be ways are in good agreement with known anatomy. compromised by missing or wrong directional informa- Conclusion: The present work shows that the advanced tion in the main diffusion eigenvector due to noise, aFM, which is especially designed for overcoming tracking partial volume effects, or, likewise, fiber crossing, limitations within areas of extensive fiber crossing, handles branching, or kissing situations (8–14). Sophisticated the fiber crossing and branching within the optic chiasm tracking algorithms have been developed recently to and the LGN correctly, thus allowing the reconstruction of overcome these limitations and to improve the tracking the entire human visual fiber pathway, from the intraor- results, e.g., by allowing fiber branching or by resolving bital segment of the optic nerves to the visual cortex. fiber crossing situations (15–20). Key Words: diffusion tensor tractography; resolving fiber Another limitation in the field of DTI fiber tracking is crossing; visual system; DTI; fast marching the lack of standardized procedures for verifying or J. Magn. Reson. Imaging 2007;26:886–893. quantifying DTI revealed connections, which makes it © 2007 Wiley-Liss, Inc. difficult to compare tracking results of different algo- rithms with each other. Anatomical variations between subjects (21–24) and missing knowledge of the exact DIFFUSION TENSOR IMAGING (DTI) (1,2) and its ap- course of fiber connections beyond the gross fiber path- plication, DTI fiber tractography (3–5), has become a ways further complicate in vivo fiber tracking evalua- prominent tool for mapping white matter axonal struc- tions. Several bundles of these main fiber connections, tures and investigating their structural integrity in the such as, e.g., the corpus callosum, superior, anterior, human brain since its introduction a decade ago. For and posterior thalamic radiations, inferior and superior fiber tracking, a variety of different tracking algorithms longitudinal fasciculi, inferior frontooccipital tract, and sagittal stratum, were reconstructed in the last few years. A summary can be found in a 3D in vivo atlas by 1Institute for Biomedical Engineering, Swiss Federal Institute of Tech- Mori et al (25) and a publication by Wakana et al (26). nology (ETH) Zurich and University Zurich, Zurich, Switzerland. An anatomically well known fiber system investigated 2Institute of Neuroradiology, University Hospital Zurich, Zurich, Swit- zerland. with DTI fiber tracking is the human visual pathway. *Address reprint requests to: P.S., Institute for Biomedical Engineering, Trip et al (27) and Iwasawa et al (28) investigated the University and ETH Zurich, Gloriastrasse 35, CH - 8092 Zurich, Swit- optic nerves in patients suffering from optic neuritis. A zerland. E-mail: staempfl[email protected],ch Received November 7, 2006; Accepted July 3, 2007. study (29) on the same disease showed pathologic DOI 10.1002/jmri.21098 changes in the optic radiation on maps generated with Published online in Wiley InterScience (www.interscience.wiley.com). the fast marching tracking technique (19). Schoth et al © 2007 Wiley-Liss, Inc. 886 DTI Fiber Tracking in Human Visual System 887 (30) explored the optic radiation in blind humans and in healthy volunteers and compared anisotropy values be- tween the two groups. Different MR techniques to ac- quire images of the optic nerve, the optic chiasm, and the optic tract have been investigated by Vinogradov et al (31). DTI fiber tracking reconstructions of the optic radiation in healthy volunteers are presented in Parker et al (19) and Staempfli et al (20). Until now, there exists no study attempting to reconstruct the entire visual pathway using DTI data. The main reasons for that are susceptibility artifacts in the area of the chiasm as well as the extensive fiber crossing within this area, which is difficult to resolve by fiber tracking algorithms. The goal of this study was to reconstruct the entire human visual pathway, from the optic nerve to the visual cortex, using a single tracking seed area, which has not been achieved until now. Therefore, the newly developed advanced fast marching algorithm (aFM) (20) was applied and its results were compared and ana- lyzed to known anatomy. A main focus was to explore the performance of the algorithm in the area of the optic chiasm. Particularly, the hypothesis being tested was whether the aFM algorithm, which was especially de- signed for resolving fiber crossings, is capable of resolv- ing this anatomically challenging situation in the hu- man visual pathway. The Human Visual System and the Visual Pathway Figure 1. Schematic depiction of the human visual system a b In this paragraph, a short summary is provided about and the visual pathway: ( ) eyes with eyeball and retina, ( ) optic nerves, (c) optic chiasm, (d) optic tracts, (e) lateral genic- the anatomy of the most important structures of the ulate nuclei (LGN), (f) superior colliculi, (g) optic radiations, human visual system. More detailed anatomical in- and (h) visual cortex. sights can be found, e.g., in Standring (32). The human visual system is subdivided into several parts (see Fig. 1). The retina (Fig. 1a), the sensory input organ of the them were scanned twice in different sessions to test visual system, transmits neural impulses through the the intrareproducibility of our results. Each subject optic nerve (Fig. 1b) to the optic chiasm (Fig. 1c), which gave informed, written consent before the study. All is positioned at the chiasmatic sulcus in the skull base, acquisitions were performed using a 3 T Achieva whole- at the junction of the anterior wall and the floor of the body system (Philips Medical Systems, Best, the Neth- third ventricle. From there, fibers of the optic nerves erlands), equipped with 80 mT/m/msec gradient coils diverge into medial and lateral hemiparts, where medial and an eight-element receive head coil array (MRI De- parts are crossing to the contralateral side and lateral vices Corp., Waukesha, WI, USA). To minimize head parts continue on the ipsilateral side of the brain within motion, the subjects were fixed in the head coil by using the optic tract (Fig. 1d). The main part of the fibers of foam padding. Additionally, they were asked to close the optic tract terminates in the lateral geniculate nu- their eyes during the acquisition to reduce eye move- cleus (LGN) (Fig. 1e). Only a few fibers pass on to the ments. superior colliculus (Fig. 1f). A main efferent fiber con- All sessions consisted of one high-resolution T1- nection from the LGN passes on via the optic radiation weighted anatomical scan and two DTI scans with dif- (Fig. 1g) and terminates in the visual cortex (Fig. 1h). ferent cardiac gating times, to investigate whether fiber Thereby, fibers first turn laterally and pass through the tracking results within the optic system are compro- sublenticular part of the internal capsule before run- mised by pulsation and motion effects. The total scan ning backward through the external sagittal stratum of time, including survey and sensitivity encoding the temporal and occipital lobes, ending within the stri- (SENSE) reference scan, added up to approximately 55 ate cortex (32,33). minutes. The anatomical data were obtained in a T1- weighted turbo field echo (TFE) scan consisting of 27 contiguous slices (field of view [FOV] ϭ 220 ϫ 220 mm2, MATERIALS AND METHODS slice thickness ϭ 0.6 mm, acquisition matrix size ϭ ϫ 2 ϭ ␣ϭ Subjects and Data Acquisition 256 256 mm ,TR 20 ms, 20°). For the DTI scans, a diffusion-weighted single-shot spin-echo echo A total of eight healthy volunteers (mean age 24.7 Ϯ 5.0 planar imaging (EPI) sequence was applied (FOV ϭ years, five female, three male) were scanned. Four of 220 ϫ 220 mm2, acquisition matrix size ϭ 96 ϫ 96, 888 Staempfli et al. reconstructed to 128 ϫ 128, contiguous slices ϭ9, slice thickness ϭ 1.8 mm, TE ϭ 45.8 msec, number of signal averages ϭ 7, partial Fourier acquisition ϭ 60%).
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