Clinical neuroanatomyAnatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data☆
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.
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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.