Thefirst descriptions of the sagittal stratum (SS) by Heinrich Sachs1,2were briefly mentioned by Déjerine in his classic book,Anatomie des Centres Nerveux.3,4Sachs used several histological techniques and studied fiber degeneration to describe this structure. The term “sagittal strata” was employed to name the white matter layers located around the atrium, occipital horn, and callosal fibers. Sachs described two layers: the stratum sagittale internum and the stratum sagittale externum. The stratum sagittale internum essentially corresponded to theoptic radiations(RADs), whereas the stratum sagittale externum only included fibers of the inferior longitudinal fasciculus (ILF). Thetapetum, made up of callosal fibers, was not included in the original description. Although advanced for that time, this anatomy needs to be revisited and updated as it was described prior to the development of Klingler’s technique, and far before the description of the inferior fronto-occipital fasciculus (iFOF) and middle longitudinal fasciculus (MdLF).5,6
The term “sagittal stratum” was adopted by Ludwig and Klingler in theirAtlas Cerebri Humanipublished in 1956.7This term is still used even if the division originally proposed by Sachs1is not. Although the term became widespread, its exact meaning remains imprecise and varies among authors.1,7–11For instance, similarly to Sachs, Fernández-Miranda et al. also consider the SS to contain an internal and an external layer.12Nevertheless, the reported contents of each layer are very different for these two authors: the stratum sagittale internum as described by Sachs in 1892 includes the RADs, whereas the internal layer of the SS was reported by Fernández-Miranda et al. in 2008 to be composed of the parietopontine and occipitopontine fibers. Similarly, the stratum sagittale externum (Sachs1) only contains ILF fibers, whereas according to Fernández-Miranda et al., the external layer of the SS only includes the RADs. According to their definition, the ILF, iFOF, and posterior limb of theanterior commissureare located lateral to the SS.1,2,12
In the present study, we used fiber dissection to investigate the composition of the SS and precisely describe the anatomical relationships among its macroscopic fasciculi in cadaveric human brains. This topic has important implications both for fundamental research and cognitive neurosciences, as well as for the development of surgical approaches for the cerebral parenchyma and ventricular system.
开云体育世界杯赔率
Twenty cerebral hemispheres obtained from the body donation programs of our institutions were employed to study SS fibers and their anatomical relationships. The bodies were prepared during the 24 hours following death.
We used a variant of the method described by Ludwig and Klingler,7in which we fixed the specimen through bilateral carotid injections of formalin before its removal from the cranial cavity, a procedure that was demonstrated to be effective in other studies performed by our team.13–15In this procedure, 1.5 L of a 4% buffered formaldehyde solution was slowly injected over 60 minutes. Intracranial fixation preserves the original shape of the brain and reduces the risk of parenchymal damage during its extraction, given the greater firmness of the tissues. The brains were then fixed for at least 2 months in formalin solution and suspended by thebasilar arteryto avoid contact with the walls of the container. The bath was changed 24 hours later to remove excess blood in the solution. Each specimen was then frozen at −20°C for at least 14 days and then slowly defrosted. To show the anatomical relationships of white matter tracts in the neighborhood of the lenticular nucleus with arteries from the anterior perforating space, themiddle cerebral arteryin each of four hemispheres was manually injected with red-colored, room temperature vulcanizing silicone with a 20-mL plastic syringe after selective catheterization and exhaustive lavage with physiological solution (NaCl 0.9%).
For exploration of the white matter and presentation of results, the 3D disposition of the main elements of the SS was exposed through progressive fiber dissection from the cortex of the lateral convexity to the ventricular system. After the gyri and sulci were studied, the gray matter—rendered fragile and friable by congelation—was delicately separated from the white matter that remained firmer. The main instruments used were handmade wooden spatulas, used to lift and progressively remove the white matter bundles. An M655 surgical microscope (Wild Heerbrugg Co.) was used as well as microsurgical instruments when the naked eye and the single or binocular loupes were no longer sufficient.
Results
Since the precise definition of SS is unclear in the literature, we decided first to describe the various layers of white matter encountered during the dissection of the temporo-parieto-occipital junction from lateral to medial, before proposing a definition for the SS.
The gray matter, darkened and made friable by the preparation, was removed to expose the subcortical short association U-fibers. The latter were removed and the posterior part of thesuperior longitudinal fasciculus(SLF)/arcuate fasciculus (AF) complex was exposed in the postero-superior portion of thetemporal lobeand in the depth of thesupramarginal gyrus, this area being the entry point for deeper dissection (Fig. 1).然后,垂直(后)和弧形排版onents of the SLF/AF complex were progressively removed. The SLF/AF was clearly distinguishable from the deeper layers as their fibers were almost perpendicular: roughly vertical for the SLF/AF in this region and horizontal for deeper fibers.
Fibers of the ILF were only observed in the inferior margin of the preparation, intermingled with other elements of the region. Although most of the ILF fibers ran at the ventral aspect of the temporal and occipital lobe, some of them could indeed be dissected from the lateral aspect. At this stage, thetemporal operculum被保留,以免消除MdLF轨迹ted superficially. The MdLF penetrated the superior temporal gyrus and planum temporale (Fig. 2A)作为一个有组织的纤维或有逐步more compact from posterior to anterior. Posteriorly, albeit superficial, the MdLF was clearly intermingled with the surrounding fibers.
Running at a deeper level than the MdLF, the iFOF reached thetemporal stemand theinsulajust posterior and dorsal to thelimen insulae. Consequently, the superior temporal gyrus including the planum temporale, and the middle temporal gyrus had to be removed prior to its dissection (Fig. 2B).的posterior segment of the iFOF was partially covered laterally by the dorsal part of the MdLF. As the dissection progressed from the posterior to the middle segment (trunk) of the iFOF, the latter ran deeper to the MdLF, reaching the antero-inferior portion of the external and extreme capsules. The ventral part of the external and extreme capsules also contained theuncinate fasciculus(UF), which was ventral to the anterior segment of the iFOF.
The optic radiations (RADs) are the next fiber contingent crossed by the dissection that originates from thelateral geniculate bodyand runs into the lateral wall of the atrium and occipital horn before reaching the lips of thecalcarine fissure(Fig. 2C and D).As proposed by Peltier et al., the RAD can be subdivided into three segments from anterior to posterior.16The first segment, or Meyer’s loop, is the most anterior and forms a posteriorly concave curve in a lateral oblique plane in close relationships with the anterior commissure and, more anteriorly, the UF. The second segment, or body of the RAD, runs along the lateral aspect of the atrium and occipital horn. Finally, the third segment joins the lips of the calcarine fissure. As a whole, the RADs—from thethalamusto the cortex—can be considered as specific posterior thalamic radiations that share the same general organization as other adjacent thalamic radiations to the occipital and parietal cortices.
Finally, the tapetum was located medial to the RADs, containing fibers in a vertical organization (Figs. 2Fand4F).This layer, which is derived from thecorpus callosum, covers the lateral aspect of the ventricular atrium and occipital horn. This was the deepest white matter layer of the lateral wall of the atrium, only limited from the CSF by the ependyma (Fig. 2F).
In summary (Figs. 3and4), the lateral wall of the ventricular atrium comprised the following elements, from medial to lateral: the ventricular ependyma, the tapetum, the RADs, the iFOF, the MdLF, the posterior portion of the SLF/AF complex, the short association U-fibers, and the cerebral cortex. Some of these elements were also present in the lateral wall of the occipital ventricular horn. The ILF only occupied the ventrolateral aspect of the dissection, its fibers contributing little to the ventral aspect of the superficial layer of the SS. Most of these structures were only partially superimposed on a sagittal plane. The MdLF, narrower than the iFOF, covered only its upper portion. The iFOF, in turn, partially covered the RADs, which overflows ventrally at the level of Meyer’s loop. The more ventrally located RADs thus exceed the area covered by the iFOF in its anterior-inferior portion and extended around thetemporal horn. As it progressed forward, the iFOF moved away from it to reach the temporal stem and the insula. Therefore, a space was created behind the directional change of the UF fibers, ahead of the Meyer’s loop and deep into the iFOF. This space was occupied by fibers from the anterior commissure, and opened in a fan of which the more caudal ones joined the SS. Although a large number of fibers were intermingled, this phenomenon varied according to the location considered. As a result, the layers could be separated at certain sites, whereas in other sites, the delamination procedure caused the fibers to rupture. For example, for the posterior segment of the iFOF, interspersed with the RADs, as both approach the occipital cortex; for the anterior commissure intermingled with those of the Meyer’s loop; and for the fibers of the anterior commissure intermingled with those of the posterior portion of the UF (Fig. 3H and I).The major white matter tracts are highlighted with colored lines inSupplementary Figs. 1–3.
Discussion
There is to date no consensus on the white matter bundles forming the SS or on its anatomical boundaries, which explains discrepancies across publications. In the present study, we used a variant of the fiber dissection technique introduced by Ludwig and Klingler7to describe the white matter layers bordering the atrium of thelateral ventricleincluding association (MdLF, iFOF, and, to a lesser degree, ILF), projection (RADs, posterior thalamic radiations), and commissural (anterior commissure) fasciculi.
We propose a definition of the SS that includes all of the white matter located between the SLF/AF complex laterally and the tapetum medially. We do not include the SLF/AF and the tapetum into the definition since their orientations (roughly vertical) clearly differ from those of the SS bundles located between (roughly horizontal). The SS was limited anteriorly by the UF and ventrally by ventral fibers of the ILF. It was not possible to establish clear dorsal and posterior anatomical boundaries, as the SS was continuous with the corona radiata up to the dorsal and posterior borders of the cerebral hemisphere.
The SS internal layer contains RADs. The RADs correspond to projection fibers of the metathalamus and thus occupy the same plane of dissection as the posterior thalamic radiations. This layer extends around the temporal ventricular horn from the lateral geniculate body, but also from the posterolateral part of the pulvinar. This was first reported in 1907 by Gustave Roussy,17who stated that “they follow a transverse and ascending course, traverse the posterior segment of the corona radiata, passing through the retro-lenticular segment of theinternal capsule, to approach, at the posterior part of the thalamus, the pulvinar and the external nucleus.” This observation was confirmed by Türe et al. using Klingler’s technique.18Moreover, Roussy, and more recently Fernández-Miranda et al.,12also drew attention to the fact that posterior thalamic radiations did not only project to the calcarine fissure, i.e., did not only include the RADs, but also wider projection fibers to the parieto-occipital cortex. The fact that the internal layer is composed only of RADs is widely but not unanimously accepted.12
A major difference between our observations and those of Sachs regards the composition of the external layer. According to Sachs, the outer layer (stratum sagittale externum) entirely corresponds to the ILF.1,2The present data clearly demonstrated that this observation overestimates the participation of this fasciculus and disregards the participation of others. Most of the ILF fibers, more exposable from the ventral aspect of the cerebral hemisphere, were situated inferiorly or relatively close to the floor of the ventricle. Only a small fiber contingent curved laterally to enter the lateral ventricular wall. As a consequence, the ILF mainly contributed to the lower part of the SS, lateral to the RADs. Conversely, the lateral layer of the SS also contained two additional fasciculi which were not originally included, the MdLF and the iFOF, which partially intermingled with the ILF.
The MdLF forms the dorsal part of the lateral layer of the SS. Its location, penetration into the temporaloperculum, and relationship to the medial aspect of the SLF/AF complex are concordant with diffusion imaging and original radioisotopic tracing studies in animals.19,20The main discrepancy, however, concerns the MdLF posterior terminations: while some diffusion imaging studies show that the MdLF ends within the angular gyrus, fiber dissection does not reproduce these results,13,19,21–23解剖水平纤维的外部er of the SS can be followed in their anteroposterior trajectory beyond that gyrus. It can be hypothesized that evolutionary changes can be the cause of these differences. In phylogeny, the thick and widely developed SLF/AF complex in humans may have moved caudally to the point where the more internal horizontal fibers curve laterally. The partial overlap of the MdLF and iFOF fascicles was also highlighted by Di Carlo et al., who introduced the term “middle layer” of the SS for the iFOF.24
A precise knowledge of the composition and spatial organization of the SS is a keystone for several surgical applications, especially temporal lobectomies and approaches to the ventricular atrium or its lateral wall.8Historically, morphological limits have been described to guide temporal lobectomies, which are still used when functional mapping techniques are not available. The rationale behind classic limits is in essence functional and is driven by the iFOF, ILF, and RADs, which partially run through the SS. With an oblique trajectory above the ventricular horn, the iFOF runs anteriorly and becomes progressively deeper in the temporal lobe, reaching the temporal stem, the insula, and finally thefrontal lobe.25Direct electrical stimulation has pointed to the role of the iFOF in language, especially semantics, in the so-called “dominant” hemisphere,8,26–28but also to the implication of its function in nonverbal semantic cognition in the “nondominant” hemisphere.29Moreover, when identified by subcortical mapping, it is a consistent landmark of where the anterolateral central (lenticulostriate) perforators from the middle cerebral artery start to be frequently encountered (Fig. 4A, B, D, and H).The ILF is suggested to be an important component for interpretation and modulation of visual input.30In the dominant hemisphere, and in conjunction with the UF, the ILF forms an indirect ventral semantic stream. Resection of the anterior part of the ILF does nevertheless not induce semantic deficits, suggesting that it is compensated for by the iFOF.31The same does not apply to posterior portions of the ILF, whose section can disconnect the visual word form area and induce severe and permanent reading disorders.32This explains the classic posterior limit for temporal lobectomy aiming at preserving this area.
The RADs also have to be considered in planning a temporal lobectomy, since a superior quadrantanopsia can follow a lesion of Meyer’s loop. They also have to be preserved in any approach to the atrium. The cortical projection of the visual field is well known: the superior lip of the calcarine fissure analyzes the lower visual fields of both eyes, whereas its inferior lip receives input from the upper visual fields. Cortical areas corresponding to the macula are located close to the occipital pole and have a bilateral representation, whereas the peripherical field of view is projected to the anterior calcarine.33
The visual field cortical areas get the following input from the geniculate body via the RADs: 1) fibers conveying inputs from the peripheral upper visual field are the most anterior ones within Meyer’s temporal loop; they curve to form the ventral part of the SS internal layer and finally reach the anterior part of the ventral lip of the calcarine fissure; 2) fibers corresponding to the macular upper visual field run more posterior within Meyer’s loop, then become dorsal to the previous fibers within the SS, and project more posteriorly (close to the occipital pole) at the ventral lip of the calcarine fissure; 3) fibers corresponding to the macular lower field run in the SS dorsal to fibers for the macular upper field and terminate in the upper calcarine lip also close to the occipital pole; and 4) fibers dedicated to the peripheral lower visual field are the most dorsal within the SS internal layer and progressively arch superiorly in the depth of the temporo-parietal junction and cover the atrium lateral to the tapetum, to finally end in the anterior part of the upper calcarine lip.
As a result, RADs in the SS correspond, from ventral to dorsal, to the peripheral upper, macular, and peripheral lower visual contralateral fields. This correspondence has to be taken into account during the planning of approaches to the temporo-parietal junction and ventricular cavity through its lateral wall. The orientation of fibers is also of interest, since incisions performed horizontally or with respect to the obliquity of fibers within the lateral ventricular wall may induce less disconnection.
目前的结果允许的系统化general organization of the SS, as well as important updates to data on the composition of the outer layer in relation to the original definitions by Sachs.1Nevertheless, there are important areas of fiber crossing between the iFOF and RADs in the posterior portion of the ventricular atrium, between the anterior commissure and Meyer’s loop, and along the ILF. As a consequence, our description is inevitably incomplete given the fact that groups of delicate and dispersed fibers may be difficult to dissect and partially destroyed during removal of the surrounding white matter. A more complete characterization of this region may emanate from the combination of complementary methods, such as ultra–high field MRI, optic coherence tomography, and polarized light imaging.
Conclusions
This study revisited the 3D organization of the white matter in the SS and shed light on certain unexplored points. Although a precise definition of its boundaries does not exist to date, we propose, based on the present results, that this region be delimited based on the surrounding white matter structures. The SS comprises the area between the SLF/AF laterally and the ventricular tapetum and ependyma medially. It is limited anteriorly by the uncinate fasciculus and inferiorly by the ILF, which is, in part, also a component of the SS. There is no precise delimitation of the superior and posterior limits as it is a continuous structure with the corona radiata and internal capsule.
This study also demonstrated the need for an update and redefinition of the classic SS composition. Diverse bundles of white matter contribute to the SS, and their spatial arrangement is highly consistent from one individual to another. That is the case for the MdLF, the iFOF, the RADs, and other posterior thalamic radiations directed to nonvisual areas of the cerebral cortex. The anterior commissure offers a small contribution to the SS anteriorly, as does the ILF inferiorly. Although a general model of SS organization in layers is possible, there are important sites of intermingling fibers that remain to be further explored.
Acknowledgments
This work was supported by the French National Agency of Research (The Fibratlas Project, ANR-14-CE17-0015) and the LE STUDIUM Loire Valley Institute for Research Studies, Orléans, France.
We would like to express our gratitude to the donors involved in the body donation program of the Association des dons du corps du Centre Ouest, Tours, who made this study possible by generously donating their bodies to science. We thank Daniel Bourry, photographer at the Université de Tours, for his technical assistance. We also thank Frank Meyer, Jean Marc Gory, Gerald Deluermoz, and Jean-Paul da Silva for their help in preparing the anatomic specimens.
Disclosures
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
Author Contributions
Conception and design: Maldonado. Acquisition of data: Maldonado, Guimarães, Cruz. Analysis and interpretation of data: Maldonado, Destrieux, Ribas, Guimarães, Cruz. Drafting the article: Maldonado. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Administrative/technical/material support: Destrieux, Ribas, Duffau. Study supervision: Maldonado.
Supplemental Information
Online-Only Content
Supplemental material is available with the online version of the article.
Supplementary Figs. 1–3.//www.prize-show.com/doi/suppl/10.3171/2020.7.JNS192846.
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