Cited by 142Advanced Neuroimaging Techniques and ApplicationsClassical Anatomy and HistologyFunctional Brain Connectivity Studies

The DOI matches its Crossref record; 41 of the 41 references it cites were found in a registry or an index; 16 of the 71 sources its claims cite were checked for support.

Cortical Terminations of the Inferior Fronto-Occipital and Uncinate Fasciculi: Anatomical Stem-Based Virtual Dissection

Open access

Abstract

We combined the neuroanatomists' approach of defining a fascicle as all fibers passing through its compact stem with diffusion-weighted tractography to investigate the cortical terminations of two association tracts, the inferior fronto-occipital fasciculus (IFOF) and the uncinate fasciculus (UF), which have recently been implicated in the ventral language circuitry. The aim was to provide a detailed and quantitative description of their terminations in 60 healthy subjects and to do so to apply an anatomical stem-based virtual dissection, mimicking classical post-mortem dissection, to extract with minimal a priori the IFOF and UF from tractography datasets. In both tracts, we consistently observed more extensive termination territories than their conventional definitions, within the middle and superior frontal, superior parietal and angular gyri for the IFOF and the middle frontal gyrus and superior, middle and inferior temporal gyri beyond the temporal pole for the UF. We revealed new insights regarding the internal organization of these tracts by investigating for the first time the frequency, distribution and hemispheric asymmetry of their terminations. Interestingly, we observed a dissociation between the lateral right-lateralized and medial left-lateralized fronto-occipital branches of the IFOF. In the UF, we observed a rightward lateralization of the orbito-frontal and temporal branches. We revealed a more detailed map of the terminations of these fiber pathways that will enable greater specificity for correlating with diseased populations and other behavioral measures. The limitations of the diffusion tensor model in this study are also discussed. We conclude that anatomical stem-based virtual dissection with diffusion tractography is a fruitful method for studying the structural anatomy of the human white matter pathways.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

Using anatomical stem-based virtual dissection of diffusion tractography in 60 healthy adults, this study maps cortical terminations of the inferior fronto-occipital fasciculus (IFOF) and uncinate fasciculus (UF) and finds more extensive territories than conventional definitions. It reports branch-specific termination frequency, density, and hemispheric asymmetries, including right-lateralized lateral IFOF/UF branches and left-lateralized medial IFOF branches.

Key findings

  • IFOF terminations extended beyond conventional definitions: inferior frontal gyrus in 100% bilaterally, lateral fronto-orbital gyrus in 87%/90% (left/right), middle frontal gyrus in 60%/55%, superior frontal gyrus in 35%/20%, and posterior regions including middle occipital gyrus 65%/95%, lingual gyrus 80%/78%, superior parietal gyrus 35%/57%, and angular gyrus 10%/33%.
  • UF terminations also extended beyond the temporal pole: medial fronto-orbital gyrus, temporal pole, and superior temporal gyrus were present in 100% bilaterally; middle temporal gyrus in 98%/97%, inferior temporal gyrus in 88%/92%, and entorhinal gyrus in 77%/78%.
  • Stem volumes were larger on the right: IFOF left 82.5 ± 35.5 mm³ vs right 100.3 ± 47.0 mm³; UF left 74.0 ± 33.0 mm³ vs right 93.9 ± 33.1 mm³ (hemisphere effect F = 40.9, p < 0.0001).
  • Asymmetry analyses showed rightward lateralization of IFOF inferior frontal and middle/inferior occipital projections, leftward lateralization of medial fronto-orbital, cuneus, and lingual IFOF projections, and rightward lateralization of UF orbito-frontal and temporal branches.

Methods

  • Diffusion-weighted MRI in 60 healthy right-handed adults (30 female; mean age 30.1, range 20–53) from the BIL&GIN database, acquired on a 3T scanner with 21 non-collinear directions (b = 1000 s/mm²), 2 mm isotropic voxels.
  • Deterministic whole-brain tractography using FACT with 0.2 fractional anisotropy and 45° angle thresholds; IFOF and UF were extracted by manual stem-based virtual dissection using modified JHU template regions of interest.
  • Termination analysis used normalized termination density scores per cortical region, a false-positive-region threshold, Wilcoxon signed-rank tests with Bonferroni correction (p < 0.0018), and asymmetry indexes tested with Bonferroni-corrected ANOVAs.

Limitations

  • The paper states that the diffusion tensor model has limited ability to resolve crossing fibers, producing broken streamlines and likely underestimating terminations, especially for the longer IFOF; it also notes that template differences may contribute to discrepancies with prior studies.
  • Evident from the text: deterministic FACT tracking, manual stem delineation, and a healthy right-handed sample restrict generalizability; the study reports no clinical or behavioral outcomes.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3389/fnana.2016.00058

Cites

41 of 41 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Figures

FIGURE 1 (A) Schemas summarizing the cortical termination territories of the IFOF (top) and UF (bottom) in the literature. The cortical territories corresponding to their conventional definitions are shown by solid black arrows and dashed gray arrows show the debated cortical territories. (B) Schemas representing the cortical termination territories of the IFOF (top) and UF (bottom) based on our stem-based tractography study. Solid lines represent the confirmed cortical territories and the regions that remain questionable are represented by dashed lines. The significant left lateralized projections are shown in blue and the right lateralized projections in red. Abbreviations: SFG, MFG, IFG, superior, middle and inferior frontal gyri; LFOG, MFOG, lateral and medial fronto-orbital gyri; RG, rectus gyrus; SOG, MOG, IOG, superior, middle and inferior occipital gyri; Cu, cuneus; LG, lingual gyrus; T. pole, temporal pole; STG, MTG, ITG, superior, middle and inferior temporal gyri; Fu, fusiform gyrus; SPG, superior parietal gyrus; AG, angular gyrus; Ent, entorhinal gyrus.
FIGURE 1 (A) Schemas summarizing the cortical termination territories of the IFOF (top) and UF (bottom) in the literature. The cortical territories corresponding to their conventional definitions are shown by solid black arrows and dashed gray arrows show the debated cortical territories. (B) Schemas representing the cortical termination territories of the IFOF (top) and UF (bottom) based on our stem-based tractography study. Solid lines represent the confirmed cortical territories and the regions that remain questionable are represented by dashed lines. The significant left lateralized projections are shown in blue and the right lateralized projections in red. Abbreviations: SFG, MFG, IFG, superior, middle and inferior frontal gyri; LFOG, MFOG, lateral and medial fronto-orbital gyri; RG, rectus gyrus; SOG, MOG, IOG, superior, middle and inferior occipital gyri; Cu, cuneus; LG, lingual gyrus; T. pole, temporal pole; STG, MTG, ITG, superior, middle and inferior temporal gyri; Fu, fusiform gyrus; SPG, superior parietal gyrus; AG, angular gyrus; Ent, entorhinal gyrus.CC BY · PubMed Central
FIGURE 2 General scheme of the different steps involved in the study from data acquisition to the extraction of the tracts using the stem-based approach to tract connectivity analysis. The temporal lobe from the JHU atlas was split to create its gray and superficial white matter pole (shown) and corresponding superior, middle and inferior divisions. The three large divisions, cortical gray matter (green), superficial white matter (yellow) and deep white matter (red), were created by combining regions of the JHU atlas, and used to select the different sub-types of streamlines.
FIGURE 2 General scheme of the different steps involved in the study from data acquisition to the extraction of the tracts using the stem-based approach to tract connectivity analysis. The temporal lobe from the JHU atlas was split to create its gray and superficial white matter pole (shown) and corresponding superior, middle and inferior divisions. The three large divisions, cortical gray matter (green), superficial white matter (yellow) and deep white matter (red), were created by combining regions of the JHU atlas, and used to select the different sub-types of streamlines.CC BY · PubMed Central
FIGURE 3 (A,B) The stem-based method. (A) The preparation of the tractogram, inspired from the postmortem dissection technique to selectively remove streamline groups not belonging to the long association pathways and (B) the procedure to delineate the stems of the IFOF and UF are shown on a single subject. Steps of the virtual dissection for the IFOF (B, first row) and UF (B, second row) with analogous images from a post-mortem dissection of the IFOF (B, third row): (i) Template regions used to remove select groups of cortical streamlines, (ii) window revealing the stem of the tract (dashed lines represent the coronal inclusion (gray) and exclusion (red) filtering slices), (iii) ROI drawn to encompass the stem of the tract, while in post-mortem dissection a red tag separates the IFOF stem from the dorsal claustrum and putamen. (C) Analogous steps from a post-mortem dissection of the IFOF (Sarubbo et al., 2013).
FIGURE 3 (A,B) The stem-based method. (A) The preparation of the tractogram, inspired from the postmortem dissection technique to selectively remove streamline groups not belonging to the long association pathways and (B) the procedure to delineate the stems of the IFOF and UF are shown on a single subject. Steps of the virtual dissection for the IFOF (B, first row) and UF (B, second row) with analogous images from a post-mortem dissection of the IFOF (B, third row): (i) Template regions used to remove select groups of cortical streamlines, (ii) window revealing the stem of the tract (dashed lines represent the coronal inclusion (gray) and exclusion (red) filtering slices), (iii) ROI drawn to encompass the stem of the tract, while in post-mortem dissection a red tag separates the IFOF stem from the dorsal claustrum and putamen. (C) Analogous steps from a post-mortem dissection of the IFOF (Sarubbo et al., 2013).CC BY · PubMed Central
FIGURE 4 The individual (first row) and mean (second row) locations of the IFOF and UF stem centers of mass are shown in MNI space projected on a single-subject T1 image from the on their mean coronal section (left) and axial sections (middle and right). The IFOF stem centers of mass are located dorsally, anteriorly and medially with respect to the UF stems.
FIGURE 4 The individual (first row) and mean (second row) locations of the IFOF and UF stem centers of mass are shown in MNI space projected on a single-subject T1 image from the on their mean coronal section (left) and axial sections (middle and right). The IFOF stem centers of mass are located dorsally, anteriorly and medially with respect to the UF stems.CC BY · PubMed Central
FIGURE 5 Examples of both left and right IFOF and UF of a typical subject extracted using the stem-based anatomical virtual dissection and shown with their stems (white). Middle top row, dorsal view of the two IFOF; middle bottom row, ventral view of the two UF.
FIGURE 5 Examples of both left and right IFOF and UF of a typical subject extracted using the stem-based anatomical virtual dissection and shown with their stems (white). Middle top row, dorsal view of the two IFOF; middle bottom row, ventral view of the two UF.CC BY · PubMed Central
FIGURE 6 The normalized termination density scores of each anterior and posterior cortical region for the IFOF and UF are shown as box plots with their means (diamonds). Abbreviations (see Figure 1).
FIGURE 6 The normalized termination density scores of each anterior and posterior cortical region for the IFOF and UF are shown as box plots with their means (diamonds). Abbreviations (see Figure 1).CC BY · PubMed Central
FIGURE 7 Mean tract termination density asymmetry indexes of the IFOF and UF showing significant lateralization for the number of streamlines.
FIGURE 7 Mean tract termination density asymmetry indexes of the IFOF and UF showing significant lateralization for the number of streamlines.CC BY · PubMed Central
FIGURE 8 Examples of the IFOF and UF tracts in a single subject segmented using different ROI-based methods: automatic template ROI sets (left; Zhang et al., 2010), obligatory passages method (middle; Catani and Thiebaut de Schotten, 2008) and the stem-based method (right, only whole anterior-to-posterior cortical streamlines are shown). The ROIs are shown in the second and fourth rows (exclusion ROIs are not shown).
FIGURE 8 Examples of the IFOF and UF tracts in a single subject segmented using different ROI-based methods: automatic template ROI sets (left; Zhang et al., 2010), obligatory passages method (middle; Catani and Thiebaut de Schotten, 2008) and the stem-based method (right, only whole anterior-to-posterior cortical streamlines are shown). The ROIs are shown in the second and fourth rows (exclusion ROIs are not shown).CC BY · PubMed Central

Verification

Claims the paper makes

79 Own result · 16 No full text of the sources · 14 Own interpretation · 7 Supported so far · 6 Not checked yet · 5 Supported · 4 No basis given · 3 Own method · 2 Partly supported · 2 Not supported · 1 Sources not found · accuracy not yet measured

Show all 73 claims

  • It may state two separate claims as one. 53
  • Probably not a substantial claim. 12
  • The quote only partly states this claim. 4
66 of 66
  • The paper relies on this without support.

    The stem of a tract is the point of passage where all fibers pass through, and extracting streamlines passing through the stem yields the complete tract.

    “we adopted the approach of neuroanatomists who first locate the stem, which is the point of passage where all fibers pass through, as an anatomical reference to identify the tract.”
  • The paper relies on this without support.

    The precentral and superior parietal gyri contain no true terminations of IFOF and UF, respectively, and can serve as false positive regions for thresholding.

    “The precentral and superior parietal gyri were chosen as the regions containing false positives (FP_REG) for the IFOF and UF, respectively.”
  • The paper relies on this without support.

    The posterior projections of the IFOF pass through the inferior longitudinal fasciculus within the temporal lobe to reach the middle occipital gyrus.

    “Similarly the posterior projections of the IFOF need to pass through the inferior longitudinal fasciculus within the temporal lobe in order to reach the middle occipital gyrus.”
3 of 3

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

2 of 2

Citations

Cites

Show all 41 references

Research works printed but not linked: 5

  1. Burdach, Vom Baue und Leben des Gehirns und Rückenmark., 1819
  2. Dejerine, 1895, Anatomie des Centres Nerveux. Tome 1.
  3. Reil, 1809, Die Sylvische Grube oder das Thal, das gestreifte grobe hirnganglium, dessen kapsel und die seitentheile des grobn gehirns., Arch. Physiol., 9, 195
  4. Trolard, 1906, Le faisceau longitudinal inférieur du cerveau., Rev. Neurol., 14, 440
  5. Wang, 2007, Diffusion toolkit: a software package for diffusion imaging data processing and tractography, Proceedings of the International Society for Magnetic Resonance in Medicine

Cited by

Sorted by citations

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Metadata

Authors
Hau, J., Sarubbo, S., Perchey, G., Crivello, F., Zago, L., Mellet, E., Jobard, G., Joliot, M., Mazoyer, B. M., Tzourio-Mazoyer, N., & Petit, L.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Ospedale Santa Chiara (IT)
Corresponding author
Petit, Laurent
Venue
Frontiers in Neuroanatomy
Published
2016-05-24
Volume
10
Pages
58-58
ISSN
1662-5129 (ISSN-L)
OpenAlex
W2401804202
Cited by
142
References
41
Citations by year
2026: 4 · 2025: 12 · 2024: 11 · 2023: 9 · 2022: 16 · 2021: 25 · 2020: 20 · 2019: 13 · 2018: 15 · 2017: 15 · 2016: 2
FWCI
11.82
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Neuroanatomy (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Research Information System (Università degli Studi di Trento) (submittedVersion, cc-by)
  • Europe PMC (PubMed Central) (submittedVersion, cc-by)
  • PubMed Central (submittedVersion, cc-by)
  • HAL (Le Centre pour la Communication Scientifique Directe) (submittedVersion, cc-by)
Funders
Agence Nationale de la Recherche (10-LABX-57, ANR-10LABX-57, ANR-10, ANR-10-LABX)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Health Sciences › Medicine › Anatomy › Classical Anatomy and Histology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords
inferior fronto-occipital fasciculus, uncinate fasciculus, association tracts, hemispheric lateralization, white matter tracts, diffusion tractography

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