Elsevier

Cortex

Volume 46, Issue 5, May 2010, Pages 691-699
Cortex

Clinical neuroanatomy
Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data

https://doi.org/10.1016/j.cortex.2009.07.015Get rights and content

Abstract

Despite electrostimulation studies of the white matter pathways, supporting the role of the inferior fronto-occipital fasciculus (IFOF) in semantic processing, little is known about the precise anatomical course of this fascicle, especially regarding its exact cortical terminations. Here, in the lights of these new functional data, we dissected 14 post-mortem human hemispheres using the Klingler fiber dissection technique, to study the IFOF fibers and to identify their actual cortical terminations in the parietal, occipital and temporal lobes. We identified two different components of the IFOF: (i) a superficial and dorsal subcomponent, which connects the frontal lobe with the superior parietal lobe and the posterior portion of the superior and middle occipital gyri, (ii) a deep and ventral subcomponent, which connects the frontal lobe with the posterior portion of the inferior occipital gyrus and the posterior temporo-basal area. Thus, our results are in line with the hypothesis of the functional role of the IFOF in the semantic system, by showing that it is mainly connected with two areas involved in semantics: the occipital associative extrastriate cortex and the temporo-basal region. Further combined anatomical (dissection and Diffusion Tensor Imaging) and functional (intraoperative subcortical stimulation) studies are needed, to clarify the exact participation of each IFOF subcomponent in semantic processing.

Introduction

In the past decade, numerous publications have addressed the issue of the functional cortical organization of the semantic system (Chao et al., 1999, Epstein et al., 1999, Haxby et al., 1999, Price, 2000, Dehaene et al., 2002, Hasson et al., 2002, McCandliss et al., 2003, Amedi et al., 2004, Cohen and Dehaene, 2004, Vihla et al., 2006). However, less attention has been given to the anatomo-functional connectivity underlying the semantic processing (Scott et al., 2000, Brugge et al., 2003). Our group has previously demonstrated that intraoperative electrical stimulation (IES) of the inferior fronto-occipital fasciculus (IFOF) induces semantic paraphasias (i.e., errors with regard to the meaning of the word target), with a high reproducibility, whatever the part of the bundle stimulated (Duffau et al., 2005, Duffau et al., 2008). Indeed, in the left frontal lobe immediately in front of and above the Broca center (Plaza et al., 2008), the anterior part of the IFOF was identified eliciting semantic paraphasias during subcortical stimulation. In the same way, in the left insula, semantic paraphasias were induced during stimulation of the intermediate portion of the IFOF, located in the ventral portion of the extreme and external capsule. Finally, in the left temporal lobe, the same type of language errors were induced by stimulation of the temporal portion of the IFOF, located above the roof of the temporal horn of the ventricle. On the basis of these observations, we have suggested that the IFOF may have an important role in the subcortical network underling the semantic system (Duffau et al., 2005, Duffau et al., 2008, Duffau, 2008).

Recent anatomical and Diffusion Tensor Imaging (DTI) works have also studied the main course of the IFOF at the level of the insula and the temporal lobe (Ture et al., 2000, Catani et al., 2002, Peuskens et al., 2004, Burgel et al., 2006, Wang et al., 2008, Catani and Thiebaut de Schotten, 2008, Fernandez-Miranda et al., 2008a, Fernandez-Miranda et al., 2008b). Nonetheless, the occipital, temporal and frontal cortical terminations of this fascicle remain a major uncertainty. Indeed, although DTI tractography enables to visualize, in vivo and non-invasively, the white matter bundles of the brain (Jones et al., 1999, Basser et al., 2000, Le Bihan et al., 2001, Mori and van Zijl, 2002, Catani et al., 2002, Catani et al., 2003, Hagmann et al., 2003, Catani et al., 2005), a major limitation of this technique is the difficulty to follow the terminal branches of the white matter pathways with reliability (Catani et al., 2003). Thus, this technique does not currently seem most adequate to analyze the cortical terminations of the IFOF. Alternatively, the technique of fiber dissection in post-mortem human brains, first described by Klingler (Klingler, 1935, Klingler and Gloor, 1960, Ludwing and Klingler, 1956), and based on freezing of the brains during the fixation process – with spreading of this freezing along the white matter fibers – allows to isolate and to follow the individual fiber bundles.

In the present work, in the lights of the recent functional data provided by intraoperative subcortical electrostimulation mapping, fiber dissection of the IFOF was performed in 14 post-mortem human hemispheres, in order to identify the exact cortical connections of this fascicle with the frontal, parietal, temporal and occipital lobes. The identification of these connections may help to better understand the exact role of this bundle in semantic processing.

Section snippets

Material and methods

Fourteen human cerebral hemispheres (7 right side and 7 left side), obtained from fresh autopsy specimens of 7 adult brains, were fixed in 10% formalin solution for at least 40 days. The pia-mater, arachnoid membrane and vascular structures were carefully removed and the hemispheres were frozen at −15 °C for 15 days. The water crystallization induced by the frozen process disrupts the structure of the gray matter (with high water content), enabling to peel off the gray matter of the brain

Initial dissection until the identification of the IFOF

First, a detailed analysis of the surface anatomy of each hemisphere is mandatory, because it will permit to identify the cortical connections of the fascicles in the last steps of the dissection. Any variability in the gyral and sulcal pattern was registered. The cortex of the depth of the sulci of the temporal, occipital, parietal and frontal lobes was removed using wooden spatulas, exposing the U-shaped fibers, which are short association fibers that interconnect the adjacent gyri (Fig. 1A

Discussion

Using the method of direct brain electrostimulation, a reliable technique of on-line anatomo-functional correlations (Duffau et al., 2002, Duffau et al., 2008, Duffau, 2008, Plaza et al., 2008, Thiebaut de Schotten et al., 2005), we have reported that stimulation of the IFOF induced semantic paraphasias, whatever the part of the bundle stimulated (occipito-temporal, insular or frontal parts) (Duffau et al., 2005). Therefore, we have suggested that the IFOF may be an important subcortical

Conclusions

Our results demonstrate that the post-mortem fiber dissection technique of human brain is an underestimated method to isolate the fibers of one specific bundle from the surrounding white matter tracts. Here, this technique enabled to identify the posterior cortical terminations of the IFOF in the parietal, occipital and temporal lobes.

Two different components of the IFOF were identified: (i) a superficial and dorsal subcomponent, which connects the frontal lobe with the superior parietal lobe

Acknowledgments

The authors wish to thank the Montpellier University of Medicine Anatomy Laboratory for its help in the preparation of the specimens.

References (61)

  • U. Hasson et al.

    Eccentricity bias as an organizing principle for human high-order object areas

    Neuron

    (2002)
  • J.V. Haxby et al.

    The effect of face inversion on activity in human neural systems for face and object perception

    Neuron

    (1999)
  • P. Indefrey et al.

    The spatial and temporal signatures of word production components

    Cognition

    (2004)
  • I.N. Lawes et al.

    Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparision with clasical dissection

    NeuroImage

    (2008)
  • B.D. McCandliss et al.

    The visual word form area: Expertise for reading in the fusiform gyrus

    Trends in Cognitive Sciences

    (2003)
  • C. Pierpaoli et al.

    Water diffusion changes in wallerian degeneration and their dependence on white matter architecture

    NeuroImage

    (2001)
  • M. Vihla et al.

    Cortical dynamics of visual/semantic vs. phonological analysis in picture confrontation

    NeuroImage

    (2006)
  • A. Amedi et al.

    Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects

    Nature Neuroscience

    (2004)
  • P. Basser et al.

    In vivo fiber tracking using DT-MRI data

    Magnetic Resonance in Medicine

    (2000)
  • J.F. Brugge et al.

    Functional connections between auditory cortex on Heschl's gyrus and on the lateral superior temporal gyrus in humans

    Journal of Neurophysiology

    (2003)
  • K. Burdach

    Vom baue und leben des gehirns und rückenmarks

    (1819)
    (1826)
  • K.O. Bushara et al.

    Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans

    Nature Neuroscience

    (1999)
  • R. Cabeza et al.

    Imaging cognition II: An empirical review of 275 PET and fMRI studies

    Journal of Cognitive Neuroscience

    (2000)
  • M. Catani et al.

    Occipito-temporal connections in the human brain

    Brain

    (2003)
  • M. Catani et al.

    Perisylvian language networks of the human brain

    Annals of Neurology

    (2005)
  • L.L. Chao et al.

    Attribute-based neural substrates in tempporal cortex for perceiving and knowing about objects

    Nature Neuroscience

    (1999)
  • C. Choi et al.

    Meyer's loop and the optic radiations in the transsylvian approach to the mediobasal temporal lobe

    Neurosurgery

    (2006)
  • Crosby EC, Humphrey T, and Lauer EW. Correlative Anatomy of the Nervous System. New York,...
  • S. Dehaene et al.

    The visual word form area: A prelexical representation of visual words in the fusiform gyrus

    NeuroReport

    (2002)
  • F. Dorrichi et al.

    White matter (dis)connections and gray matter (dys)functions in visual neglect: Gaining insights into the brain networks of spatial awareness

    Cortex

    (2008)
  • Cited by (385)

    View all citing articles on Scopus

    Sources of financial support: Juan Martino receives specific founding from the Post-MIR Wenceslao López-Albo's grant. Fundación “Marqués de Valdecilla”, IFIMAV, Santander, Cantabria, Spain.

    View full text