Feasibility of creating a high-resolution 3D diffusion tensor imaging based atlas of the human brainstem: a case study at 11.7 T - PubMed (original) (raw)

Feasibility of creating a high-resolution 3D diffusion tensor imaging based atlas of the human brainstem: a case study at 11.7 T

Manisha Aggarwal et al. Neuroimage. 2013.

Abstract

A three-dimensional stereotaxic atlas of the human brainstem based on high resolution ex vivo diffusion tensor imaging (DTI) is introduced. The atlas consists of high resolution (125-255 μm isotropic) three-dimensional DT images of the formalin-fixed brainstem acquired at 11.7 T. The DTI data revealed microscopic neuroanatomical details, allowing three-dimensional visualization and reconstruction of fiber pathways including the decussation of the pyramidal tract fibers, and interdigitating fascicles of the corticospinal and transverse pontine fibers. Additionally, strong gray-white matter contrasts in the apparent diffusion coefficient (ADC) maps enabled precise delineation of gray matter nuclei in the brainstem, including the cranial nerve and the inferior olivary nuclei. Comparison with myelin-stained histology shows that at the level of resolution achieved in this study, the structural details resolved with DTI contrasts in the brainstem were comparable to anatomical delineation obtained with histological sectioning. Major neural structures delineated from DTI contrasts in the brainstem are segmented and three-dimensionally reconstructed. Further, the ex vivo DTI data are nonlinearly mapped to a widely-used in vivo human brain atlas, to construct a high-resolution atlas of the brainstem in the Montreal Neurological Institute (MNI) stereotaxic coordinate space. The results demonstrate the feasibility of developing a 3D DTI based atlas for detailed characterization of brainstem neuroanatomy with high resolution and contrasts, which will be a useful resource for research and clinical applications.

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Figures

Fig. 1

DTI of the ex vivo brainstem at 255 μm isotropic resolution. Sagittal and axial sections from the direction-encoded colormap (DEC) derived from DTI are shown. Corresponding T2-weighted (T2-wt) axial sections are shown for anatomic comparison. In the DEC maps, red, blue and green represent anisotropy along medial-lateral, superior-inferior, and anterior-posterior orientations, respectively. Abbreviations used are: CST: corticospinal tract, ML: medial lemniscus, mlf: medial longitudinal fasciculus, MCP: middle cerebellar peduncle, SCP: superior cerebellar peduncle, DSCP: decussation of the superior cerebellar peduncle, tpf: transverse pontine fibers. Scale bar = 4 mm.

Fig. 2

Neuroanatomical details in the brainstem resolved with the high-resolution ex vivo DTI. Sagittal (a, b) and coronal (c, d) sections from DEC maps show the different structures delineated at each level. The anatomic locations of the sections are indicated in corresponding scout in vivo brain images. Red, green and blue represent anisotropy along medial-lateral, anterior-posterior, and superior-inferior orientations, respectively. Structural abbreviations are: CST: corticospinal tract, CTT: central tegmental tract, DSCP: decussation of the superior cerebellar peduncle, ML: medial lemniscus, mlf: medial longitudinal fasciculus, PC: posterior commissure, SCP: superior cerebellar peduncle, TB: trapezoid body, tpf: transverse pontine fibers.

Fig. 3

Three-dimensional reconstruction of brainstem nuclei and white matter tracts from the DTI data. a) Reconstructed cranial nerve and inferior olivary nuclei are overlaid on the ADC map for anatomic reference. The pontine nuclei in the basal pons are visible as hyperintense bands in the ADC map (inset). b–d) Three-dimensional rendering of fibers reconstructed from tractography are overlaid on fractional anisotropy images for anatomic reference, with color representing the orientations of the fibers. Red, green and blue indicate fiber orientations along the medial-lateral, anterior-posterior, and superior-inferior axes, respectively. Abbreviations are: III n: oculomotor nucleus, IV n: trochlear nucleus, Vp: primary sensory nucleus of trigeminal nerve, Vm: trigeminal motor nucleus, VI n: abducens nucleus, VII n: facial motor nucleus, CN V: trigeminal nerve, CST: corticospinal tract, IO: inferior olivary nucleus, LVN: lateral vestibular nucleus, MCP: middle cerebellar peduncle, ML: medial lemniscus, pn: pontine nuclei, SCP: superior cerebellar peduncle, tpf: transverse pontine fibers.

Fig. 4

Anatomical details in the medulla oblongata resolved with ex vivo DTI at 170 μm isotropic resolution. a) Axial (top panel) and coronal (bottom panel) sections through the medulla show isotropic diffusion-weighted (iDW), apparent diffusion coefficient (ADC), and direction encoded colormap (DEC) contrasts derived from DTI. In the DEC maps, red, blue and green represent anisotropy along medial-lateral, superior-inferior, and anterior-posterior orientations, respectively. Scale bar = 4 mm. b) Three-dimensional reconstruction of fiber tracts and nuclei in the medulla from the tensor data. Tracts reconstructed using tractography are color-coded based on fiber orientations and shown in a sagittal view in the left panel. Red, green and blue denote fiber orientations along medial-lateral, anterior-posterior, and superior-inferior axes, respectively. The right panel shows 3D rendering of grey matter nuclei and the pyramidal tract overlaid on the ADC map for anatomical reference. VI n: abducens nucleus, XII n: hypoglossal nucleus, DAO: dorsal accessory olivary nucleus, IO: inferior olivary complex, MAO: medial accessory olivary nucleus, ML: medial lemniscus, mlf: medial longitudinal fasciculus, NC: nucleus cuneatus, ocf: olivocerebellar fibers, PO: primary olivary nucleus, Py: pyramids, PyD: pyramidal decussation, sol: solitary tract, spV: spinal trigeminal tract, STT: spinothalamic tract.

Fig. 5

Ex vivo DTI of the cervical spinal cord at the level of the spinomedullary junction showing the decussation of the pyramidal tracts (PyD). a–b) Coronal and axial sections through the DEC maps show delineation of the PyD and medial longitudinal fasciculus (mlf). Scale bar = 2 mm. c–d) Fiber tractography shows interdigitating bundles from the left and right pyramidal (Py) tracts (reconstructed fibers are cropped to coronal and axial sections in c and d, respectively). Fibers are colored by orientation, with red, green and blue denoting fiber orientations along medial-lateral, anterior-posterior, and superior-inferior axes, respectively. e) Three-dimensional reconstruction of the left pyramidal tract (rendered in blue), showing crossed fibers forming the lateral corticospinal tract (LCST) and uncrossed pyramidal fibers continuing into the ipsilateral anterior corticospinal tract (aCST).

Fig. 6

Fig. 6a. Comparison of DTI contrasts in the brainstem with myelin-stained histology. The left panel shows DEC maps of axial sections at the level of the caudal medulla (a), rostral medulla (b), and caudal pons (c). Corresponding histology sections from Nolte’s human brain atlas (Nolte, 2008) are shown in the right panel (reproduced with permission). Structural abbreviations are: 4V: fourth ventricle, XII N: hypoglossal nucleus, cc: central canal, CN XII: hypoglossal nerve, CST: corticospinal tract, CTT: central tegmental tract, FC: fasciculus cuneatus, iaf: internal arcuate fibers, ICP: inferior cerebellar peduncle, IO: inferior olivary nucleus, LNC: lateral cuneatus nucleus, MAO: medial accessory olivary nucleus, MCP: middle cerebellar peduncle, ML: medial lemniscus, mlf: medial longitudinal fasciculus, NC: nucleus cuneatus, NG: nucleus gracilis, ocf: olivocerebellar fibers, Py: pyramid, RF: reticular formation, RN: raphe nuclei, SO: superior olivary nucleus, sol: solitary tract, SpV: spinal trigeminal tract, STT: spinothalamic tract, TB: trapezoid body, tpf: transverse pontine fibers, vsc: ventral spinocerebellar tract. Fig. 6b. Comparison of DTI contrasts in the brainstem with myelin-stained histology. The left panel shows DEC maps of axial sections at the level of the midpons (d), rostral pons (e), and caudal midbrain (f). Corresponding histology sections from Nolte’s human brain atlas (Nolte, 2008) are shown in the right panel (reproduced with permission). Structural abbreviations are: CN V: trigeminal nerve, CP: cerebral peduncle, CST: corticospinal tract, CTT: central tegmental tract, dlf: dorsal longitudinal fasciculus, DRN: dorsal raphe nucleus, DSCP: decussation of the superior cerebellar peduncles, LL: lateral lemniscus, MCP: middle cerebellar peduncle, ML: medial lemniscus, mlf: medial longitudinal fasciculus, RF: reticular formation, RN: raphe nuclei, SCP: superior cerebellar peduncle, tpf: transverse pontine fibers.

Fig. 6

Fig. 7

Co-registration of the high-resolution ex vivo brainstem DTI data to the JHU in vivo brain atlas (Oishi et al., 2011). A representative coronal section (y = −26 mm in MNI coordinates) through the in vivo atlas (a) and the corresponding co-registered section from the ex vivo data (b) show the degree of registration accuracy. The color-coded map of the Jacobian determinant overlaid on the anatomical image (c) represents the local volumetric scaling applied by the transformation to warp the ex vivo data to the in vivo atlas. In the Jacobian map, values greater than 1 represent local expansion, and values less than 1 represent local volumetric contraction of the ex vivo image under the deformation. Scales shown are in units of mm with 10 mm spacing.

Fig. 8

The high-resolution DTI atlas of the brainstem registered to the MNI stereotaxic coordinate space. Orthogonal planar views from the in vivo whole-brain atlas (2.2 mm resolution) and corresponding sections through the constructed brainstem atlas (0.225 mm resolution) are shown for comparison of anatomical details. Red, green and blue in the DEC maps represent anisotropy orientation along the medial-lateral, anterior-posterior, and superior-inferior axes, respectively. All scales are in units of mm.

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Feasibility of creating a high-resolution 3D diffusion tensor imaging based atlas of the human brainstem: a case study at 11.7 T - PubMed (original) (raw)