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| REVIEW ARTICLE |
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| Year : 2021 | Volume
: 4
| Issue : 3 | Page : 3-13 |
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Gliomas are confined to a fiber tract – Concept and clinical implications
Abhidha Shah, Sukhdeep Singh Jhawar, Atul Goel
Department of Neurosurgery, KEM Hospital and Seth GS Medical College, Mumbai, Maharashtra, India
| Date of Web Publication | 02-Nov-2021 |
Correspondence Address:
Dr. Abhidha Shah
Department of Neurosurgery, KEM Hospital and Seth GS Medical College, Parel, Mumbai - 400 012, Maharashtra
India
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/IJNO.IJNO_401_21
A novel classification of white fibers of the brain has been proposed based on the direction and depth of the various fiber bundles. The implications of this classification for glioma surgery are presented. Using fiber dissection techniques described by Klingler, the various association, commissural and projection fiber bundles of the brain were studied. The fibers were studied by the naked eye and with the use of magnification. The white fibers of the cerebrum were divided architecturally into five groups- four horizontal groups and one vertical group, based on three dimensional understanding of the white fibers. The four horizontal groups are the superficial, middle, deep and central groups and the vertical group included the projection fibres. The association fibers constitute the superficial, middle and deep groups. The commissural fibers form the central group. In this article, the course of the major fiber bundles of the brain is discussed. The cortical structures and subcortical networks that are involved in major human functions are presented. The implications of the proposed classification of white fibers in the surgical management of gliomas are discussed. Deciphering the cortical and subcortical anatomy of the brain is crucial to avoid neurological morbidity while performing intra-axial brain tumor surgery.
Keywords: Fiber dissection, Klingler's technique, function, white fibers
How to cite this article:
Shah A, Jhawar SS, Goel A. Gliomas are confined to a fiber tract – Concept and clinical implications. Int J Neurooncol 2021;4, Suppl S1:3-13 |
| Introduction | |  |
You have to learn the rules of the game and then play better than anyone else.
– Albert Einstein.
This quote has utmost relevance in the field of neuro-oncology where surgery involves a balancing act between radical resection and no neurological morbidity. Currently, various preoperative and intraoperative adjuncts are available to aid in planning and performing safe surgery for intra-axial brain tumors. Although these form useful technical guides, understanding cortical and subcortical anatomy and function has come to play a defining role in surgical neuro-oncology. The traditionalist viewpoint considered only cortical areas for eloquence; however, with the concept of connectome, various subcortical networks have been identified which are essential for function. Whilst damage to a cortical area can be compensated for by another area by neuronal plasticity, damage to white fiber bundles is irrevocable. Hence, understanding of subcortical anatomy and function is crucial before embarking on intra-axial brain surgery. In this article, we discuss our novel classification of white fibers of the brain, which we believe is useful in three-dimensional understanding of the subcortical neural architecture.[1] We also present cortical and subcortical substrates of some higher order functional networks. On the basis of our clinical studies, we identify that gliomas arise from and are located within the confines of a named white fiber tract and the adjoining tracts are involved by virtue of displacement and distortion and not by destruction and demolition.[2],[3]
| Specimen Preparation and Steps of Dissection | | |
All the dissections were performed in the microneurosurgical laboratory of the Seth G.S. Medical College and K.E.M Hospital, Mumbai. The specimens were prepared using Klingler's method for studying white fiber anatomy.[1],[4],[5] Formalin-fixed cadaveric human brain specimens were frozen at –10° for 4–6 weeks. The specimens were then thawed under normal temperature water for 24 hours. After thawing, the brain was stripped of its pia and the underlying vessels until a bare cortical surface was obtained. The dissection was then commenced. The gyri and sulci on the surface of the brain were delineated. Initially, the thin layer of cortex on the entire surface of the hemisphere was peeled away. Once this layer is removed, a distinctive layer of white matter is seen in the center of the gyrus surrounded by the gray matter. This gray matter, which runs in the depths of the sulci, is then cored out over the entire hemisphere. This reveals the short association or the U fibers. Further dissection then proceeds via three approaches: lateral, medial, and inferior. The white fibers beneath each named gyri were identified and the entire course of the named white fiber tract was delineated.
| Classification of White Fibers of the Brain | | |
We recently published a novel classification of the structural design of the white fibers of the brain based on the direction and depth of the fiber bundles.[1] We believe that this will help both the novice and the trained neurosurgeon in understanding the intangible anatomy of the white fibers of the brain and in preventing neurological deficits.
Architecturally, the white fibers of the brain can be divided into five groups (four horizontal and one vertical group)[1] [Figure 1]. The four horizontal layers are the superficial group, the middle group, the deep group, and the central group.[1] The first horizontal layer or the superficial group is that of the short association fibers, the U fibers, or the intergyral fibers. This layer is present through the entirety of the cerebral hemisphere and only after its removal can the next level be approached. The second horizontal layer or the middle group is that of the long association fibers that connect various regions of the cerebral hemispheres. These are the superior longitudinal fasciculus (SLF), the arcuate fasciculus (AF), the middle longitudinal fasciculus, the inferior longitudinal fasciculus (ILF) and the cingulum. Further in depth are the uncinate fasciculus (UF), the inferior fronto-occipital fasciculus (IFOF), and the sagittal stratum.[1] The third horizontal layer or the deep group of fibers is that of the deep association fibers. These fibers lie within the ventricular system and in close relation to the walls of the ventricular cavity. The other characteristic of most of these fibers is that they run in a distinctive “C” formation. These are the fornix, the stria terminalis, the striae medullaris thalami, and the medial and longitudinal striae. There are 2 other fiber bundles that lie within the gray matter of the thalamus and the upper midbrain, which are included here. These are the mammillothalamic and the mammillotegmental tracts. The central group of fibers comprises the commissural fibers, which connect the two hemispheres to each other across the midline. These are the corpus callosum, the anterior commissure, the posterior commissure, the habenular commissure, and the hippocampal commissure. The vertical group of fibers are the projection fibers, which run rostral to caudal, connecting the cortex to the diencephalon and the brainstem. These are the internal capsule and the thalamic radiations. The vertical group of fibers divides the white fibers of the hemisphere into medial and lateral halves. Fibers that are medial to the vertical group do not cross over to the lateral side and those that are lateral to the vertical group do not cross over to the medial side. The only exception is the anterior commissure that traverses below and anterior to the vertical group of fibers as it enters the temporal brain. The deep gray matter of the brain lies straddled on both sides of the vertical group of projection fibers. The central group or the commissural fibers lie between the vertical layer of the projection fibers of both the hemispheres. | Figure 1: Dissected specimen of the medial aspect of cerebral hemisphere showing the classification of the various fiber bundles. The circles denote the various levels or groups. The first horizontal layer (red circle) or the superficial group is that of the short association fibers, the U fibers, or the intergyral fibers. The second horizontal layer (purple circle) or the middle group is that of the long association fibers. On the medial surface, these consist of the superior longitudinal fasciculus and the cingulum. The central group (blue circle) is that of the commissural fibers that run from one hemisphere horizontally to the other. On the medial surface, the corpus callosum constitutes the central group. The vertical group (orange circle) of fibers is that of the projection fibers. These comprise the internal capsule and the thalamic radiations. On the medial surface of the hemisphere, this is represented by the corona radiata. The third horizontal layer (yellow circle) or the deep group of fibers is that of the deep association fibers. These fibers lie within the ventricular system in close relation to the walls of the ventricular cavity. These are the fornix, the stria terminalis, striae medullaris thalami, and the medial and longitudinal striae
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| Course and Connections of Important Fiber Bundles in the Various Layers | | |
The first layer/superficial group
Short association or U fibers
The superficial group consists of the short association or U fibers. They are present over the entire surface of the brain and can be visualized after coring out the gray matter interconnecting the nearby gyri to each other [Figure 2]. The short arcuate fibers run vertically to a depth of about 2 to 2.5 cm.[1] | Figure 2: The superior surface of the cerebral hemisphere. On one side the gray matter has been kept intact. On the other side the superficial cortical gray matter in the depths of the sulci has been removed to show the short arcuate fibers
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The second layer/the middle group
Superior longitudinal fasciculus
The SLF is the most superficial and the first of the long association fibers to be encountered after removal of the short association fibers. It runs between the frontal and parietal lobes [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]. The superior longitudinal fasciculus and the AF were considered as part of a single fiber system by various authors and described as a single structure with a horizontal frontoparietal segment, a vertical temporoparietal segment, and a horizontal frontotemporal segment or the AF.[6],[7] Rhoton et al. described the superior longitudinal fasciculus as having three parts: SLF- I, SLF – II, and SLF – III from medial to lateral.[8] Our dissections have revealed that the superior longitudinal fasciculus connects the frontal and parietal lobes and consists of two parts, namely the medial SLF and the lateral SLF which lie on either side of the projection fibers.[1],[9] The medial part of the SLF (also known as the SLF-I) begins at the superior frontal gyrus and runs posteriorly to reach the precuneus in the parietal lobe.[1] It runs above the cingulum and its lateral relations are the dorsal radiations of the corpus callosum and the corona radiata. The lateral part of the superior longitudinal fasciculus (SLF-II and SLF-III) connects the middle frontal gyrus to the angular gyrus (SLF-II) and the inferior frontal gyrus to the supramarginal gyrus (SLF-III). It is not very easy to separate these two portions of the SLF as they run between the frontal and parietal lobes as a confluent bundle.[1] The AF lies ventral to this portion of the lateral portion of the SLF. | Figure 3: Dissected specimen showing the fibers on the lateral aspect of the hemisphere. The superior, middle, inferior frontal gyri, the precentral and postcentral gyri, the superior and inferior parietal lobules, the superior temporal gyrus, and the occipital gyri have been removed to reveal the following fiber bundles. (a) Vertical fibers of the corona radiata, (b) the lateral portion of the superior longitudinal fasciculus (SLF II and III), (c) Arcuate fasciculus, (d) Inferior fronto-occipital fasciculus, e. Uncinate fasciculus, (f) Dorsal external capsule, (g) External capsule as it courses below the AF to form corona radiata, (h) Putamen, (i) Inferior longitudinal fasciculus
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 | Figure 4: Lateral view of the hemisphere after removal of gray matter of the entire hemisphere. (a) Corona radiata, (b) lateral portion of superior longitudinal fasciculus (SLF-II and SLF-III), (c) arcuate fasciculus, (d) inferior fronto-occipital fasciculus, (e) uncinate fasciculus, (f) dorsal external capsule, (g) inferior longitudinal fasciculus, (h) optic radiations
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 | Figure 5: Dissected specimen showing the entire extent of the internal capsule and the vertical layer of projection fibers. (a) Anterior limb of the internal capsule, (b) Genu of the internal capsule, (c) Posterior limb of the internal capsule, (d) Retrolenticular portion of the internal capsule, (e) Sublenticular portion of the internal capsule (Meyer's loop)
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 | Figure 6: Tractography image showing the various fiber bundles. IFOF: Inferior fronto-occipital fasciculus, ILF: Inferior longitudinal fasciculus, AF: Arcuate fasciculus, SS: Sagittal stratum, IC: Internal capsule
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 | Figure 7: :Supero-lateral view of the dissected specimen. (a) Corona radiata, (b) Lateral portion of superior longitudinal fasciculus (SLF-II and SLF-III), (c) Arcuate fasciculus, (d) Inferior fronto-occipital fasciculus, (e) Optic radiations. Note that fibers lateral to the vertical group (projection fibers/corona radiata) remain lateral and do not cross the vertical group
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Arcuate fasciculus
The AF is a reverse C-shaped fiber bundle that has been traditionally known to connect the inferior frontal gyrus (Broca's area) and the posterior portion of the superior temporal gyrus (Wernicke's area)[1] [Figure 3], [Figure 4], [Figure 5], [Figure 6]. In our dissections, the AF was visualized as running beneath the lateral portion of the SLF in the frontal and parietal region, then curving downward in the region of the supramarginal and angular gyrus, and then running forward toward the posterior portion of the superior temporal gyrus[1] [Figure 3]. Thus, the AF wraps around the posterior edge of the insula in a horseshoe-like configuration beneath the frontal, parietal and temporal opercula and connects the middle and superior temporal gyri to the inferior and middle frontal gyri. It runs beneath the inferior portion of the superior temporal gyrus, the superior portion of the middle temporal gyrus, the angular and supramarginal gyri, the supra-Sylvian portions of the pre- and post-central gyri, and the posterior parts of the middle and inferior frontal gyri.[1],[10],[11]
Ventral occipital fasciculus
This fasciculus runs just posterior to the turn of the AF. It connects the inferior occipital lobe to the superior occipital lobe and the angular gyrus.[1]
Middle longitudinal fasciculus
The existence of the middle longitudinal fasciculus in humans was much debated but its existence has been clearly demonstrated in recent fiber dissection studies.[10] The middle longitudinal fasciculus connects the superior temporal lobe with the parietal lobe and can be visualized by removing the fibers of the AF. The fibers run posteriorly and slightly superiorly toward the parietal and occipital lobes but do not have a clear termination. They form the uppermost portion of the sagittal stratum.
Inferior longitudinal fasciculus
The ILF connects the inferior parts of the temporal and occipital lobes and can be visualized after removing the gray matter of the inferior temporal gyrus and the fusiform gyrus[1] [Figure 3] and [Figure 4]. It is seen beneath the inferior temporal gyrus coursing toward the inferior portion of the occipital lobe.
Inferior fronto-occipital fasciculus
Fibers from the lateral orbital gyri join fibers from the middle and inferior frontal gyri to form the inferior fronto-occipital fasciculus (IFOF) [Figure 4], [Figure 5], [Figure 6], [Figure 7]. All the fibers aggregate and pass inferior to the corona radiata fibers and beneath the lateral portion of the SLF and AF toward the temporal lobe as a constituent of the temporal stem[1] [Figure 4]. After exiting the temporal stem, the majority of the IFOF passes through the superior and middle temporal gyri to reach the parietal and occipital gyri. Some fibers of the IFOF turn anteriorly along with the UF to end in the superior and middle temporal gyri. The fibers of the IFOF running posteriorly form a major component of the sagittal stratum and lie lateral to the optic radiations.[1]
Uncinate fasciculus
The uncinate fasciculus (UF) along with the IFOF forms a constituent of the temporal stem connecting the orbitofrontal and temporal regions. The UF originates in the medial and lateral orbital gyri, runs anteroinferior to the IFOF in the temporal stem, and ends in the anterior aspect of the superior and middle temporal gyri [Figure 4], [Figure 5], [Figure 6], [Figure 7]. The dorsolateral portion of the UF connects the temporal pole to the lateral orbitofrontal gyri and its ventromedial portion connects the temporal pole to the medial orbitofrontal cortex and the septal area. The frontal portion of the UF runs anterior to the anterior perforated substance deep to the posterior orbital gyrus. It covers the infero-medial portion of the nucleus accumbens and ultimately terminates in the region below the genu of the corpus callosum.
Sagittal stratum and the optic radiations
The sagittal stratum, as the name suggests, is a series of layers of fibers that can be seen running from the posterior temporal region to the occipital lobe, deep to the AF. [Figure 4] and [Figure 5]. It consists of a series of parallel running fibers, which are the MLF, the IFOF, the fibers of the anterior commissure and the optic radiations, and the tapetum. The IFOF, fibers of the AF, and the optic radiations form the bulk of the sagittal stratum. [11],[12],[13] Although these three fiber systems are difficult to distinguish after they merge with the optic radiations, we have found that the fibers of the anterior commissure and the IFOF lie laterally and the optic radiations lie medially.[1],[13] The point where the three fiber systems converge was clearly identified in our fiber dissection previously.[13] At the point of intersection, the fibers of the IFOF, the anterior commissure, and the Meyer's loop can be identified, from lateral to the medial aspect. The optic radiations or the geniculocalcarine tract originates at the lateral geniculate body and ends in the calcarine cortex on the medial aspect of the occipital lobe. The optic radiations are composed of three bundles, anterior, central, and posterior. [Figure 4] and [Figure 7]. Though by the general direction of the fiber bundles three main bundles can be distinguished, it is not usually possible to clearly delineate the three bundles.[1],[13] The anterior bundle, also known as the Meyer's loop, travels anteriorly from the lateral geniculate body to the roof of the temporal horn and then turns posteriorly in the lateral wall of the temporal horn. It continues posteriorly to terminate at the inferior bank of the calcarine sulcus within the lingual gyrus. The central bundle courses laterally over the roof of the temporal horn and then courses posteriorly in the lateral wall of the trigone and occipital horn. It terminates at the occipital pole. The posterior bundle travels directly posteriorly over the trigone as part of its lateral wall and roof to end in the superior bank of the calcarine sulcus within the cuneus.[13]
Cingulum
The cingulum is a C-shaped association bundle which runs just above and parallel to the corpus callosum.[5] The cingulum originates below the rostrum of the corpus callosum in the region of the subcallosal gyrus[1] [Figure 8] and [Figure 9]. It then runs superiorly around the curve of the genu of the corpus callosum and then continues posteriorly. Above the splenium, the cingulum narrows to form the isthmus of the cingulum, which continues below as the radiation of the cingulum to end in the anterior parahippocampal region adjacent to the hippocampus. The cingulum from its superior surface sends connections to the frontal and parietal cortices. Two of these connections are very clearly depicted in [Figure 9]. The cingulum forms a major component of the limbic system and the Papez circuit. | Figure 8: Supero-medial view of the dissected specimen. (a) Medial part of the SLF (SLF-I), (b) Cingulum, (c) Corpus callosum, (d) Short arcuate fibers, (e) Caudate head
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 | Figure 9: Medial surface of the hemisphere after removal of the cortical gray matter. (a) Corona radiata, (b) cingulum, (c) corpus callosum, (d) fibers of the corpus callosum as they turn superiorly medial to the corona radiate, (e) Radiation of the cingulum as it ends in the parahippocampal region, (f) caudate head, (g) fornix
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Medial and lateral olfactory striae
The medial and lateral olfactory striae represent the terminations of the olfactory tract on the basal surface of the frontal lobe.[1] The lateral olfactory stria forms the anterolateral border of the anterior perforated substance. The lateral olfactory stria and gyrus pass along the lateral margin of the anterior perforated substance to reach the piriform region.[5],[14] These fibers terminate in the piriform cortex and the corticomedial part of the amygdaloid nuclear complex. The medial olfactory stria becomes continuous with the subcallosal and the paraterminal gyrus. The subcallosal area and the paraterminal gyrus constitute the septal area, beneath which are the septal nuclei.[5],[14] The septal region is situated on the medial surface of the cerebral hemisphere, immediately facing the anterior commissure. The medial septal nucleus becomes continuous with the nucleus and tract of the diagonal band of Broca, which then connects with the hippocampal formation and the amygdala. Thus, the diagonal band of Broca connects the amygdala to the medial septal region.
The central group
Corpus callosum
The corpus callosum is the largest commissural fiber system of the brain. When viewed on the medial surface of the brain, it appears as a horizontally placed letter “C” [Figure 10]. It is divided into 4 parts, the rostrum, the genu, the body, and the splenium. Superiorly, a thin sheet of gray matter, the indusium griseum, covers the surface of the corpus callosum. The indusium griseum is the continuation of the subsplenial gyrus on the surface of the corpus callosum, which ends in the subcallosal region. Within the indusium, griseum are two longitudinal striae called the medial and longitudinal striae of Lancisi.[1],[5] These fibers are considered to be aberrant fibers of the fornix, which leave the fimbria, course over the superior surface of the corpus callosum, and then join the fornix again anteriorly. Once this layer is removed the transverse running fibers of the corpus callosum are visualized. The transverse running fibers of the corpus callosum curve superiorly and inferiorly and when viewed from a posterior perspective, resemble two horizontally placed letters “C” placed one on top of the other.[1] When viewed from above, the fibers of the corpus callosum resemble upturned bicycle handles running from one corona radiata to the other corona radiata connecting both the hemispheres.[1] Thus, the corpus callosum lies between the vertical layer of fibers in each hemisphere. This whole constellation of fibers of the horizontal spread of the corpus callosum and the two vertical fiber layers of the projection system on each side resembles a hanging rope bridge.[1] Unlike a rope bridge, however, the transfer of information occurs from side to side rather than from anterior to posterior. The fibers of the corpus callosum after crossing the cingulum turn anteriorly, superiorly, posteriorly, and inferiorly to form the anterior, dorsal, posterior, and ventral callosal radiations. The fibers arising from the genu of the corpus callosum curve anteriorly to form the anterior callosal radiation or the forceps minor. The forceps minor connects the prefrontal and the orbitofrontal areas and forms the medial wall of the frontal horn of the lateral ventricle. The callosal fibers emanating from the rostrum form the floor of the frontal horn of the lateral ventricle. These fibers reach the temporal stem on either side of the hemisphere thus connecting the temporal lobes. The dorsal callosal radiations consist of horizontal fibers from the body of the corpus callosum that course laterally and then curve upward to merge with the fibers of the corona radiata. They connect the frontal and parietal lobes of each hemisphere to the other. The callosal fibers of the splenium, curve posteriorly to form the posterior callosal radiations or the forceps major. The forceps major connect the occipital lobes to each other. They form a bulge in the medial wall of the atrium of the lateral ventricle. The ventral fibers emerging from the genu of the corpus callosum form the anteromedial portion of the medial wall of the frontal horn. These fibers also connect bilateral caudate nuclei to each other.[1] The ventral fibers arising from the body of the corpus callosum curve inferiorly and form the roof of the superior part of the frontal horn and the body of the lateral ventricle. These fibres also connect bilateral caudate nuclei to each other.[1] The ventral sheet of fibers that arise from the ventral portion of the splenium run laterally and then curve downward to form the superior and lateral wall of the atrium and temporal horn. These fibers are known as the tapetum. They separate the temporal and the atrial lateral walls from the optic radiations. Thus, the corpus callosum connects similar regions of the hemispheres to each other. It also encompasses the entire ventricular system within its callosal radiations. | Figure 10: Image showing the entire antero-posterior extent of the corpus callosum. (a) Transverse running fibers of the corpus callosum, (b) Fibers of the corpus callosum as they curve upwards on the medial aspect of the cerebral hemisphere
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Anterior commissure
The anterior commissure resembles a horizontally placed bow and runs anterior to the columns of the fornix[1],[5],[13],[14] [Figure 11]. The anterior commissure runs in a canal of gray matter (canal of Gratiolet) parallel and deep to the UF and the IFOF.[1] It lies deep to the anterior perforated substance. The fibers of the anterior commissure divide into an anterior and posterior component. Only a small bulk of the fibers run anteriorly while most of the compact bulk of this white fiber tract runs posteriorly. The anterior fibers connect the anterior olfactory nucleus of one side to the contralateral side. The posterior portion of the anterior commissure runs posterolaterally deep to the lentiform nucleus and middle temporal gyrus and ultimately forms a component of the sagittal stratum. The globus pallidus lies posterior to the temporal component of the anterior commissure. As discussed earlier, the anterior commissure is the only fiber bundle that crosses the vertical layer of the projection system. | Figure 11: Dissection of the basal surface of the brain. (a) Anterior commissure, (b) optic tract, (c) mammillary body, (d) cerebral peduncle. (e) ventro-medial portion of the uncinate fasciculus, (f) Inferior fronto-occipital fasciculus, (g) Substantia innominate
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Hippocampal commissure/psalterium
The psalterium (named after an ancient stringed instrument) has been known by various names such as the hippocampal fissure, the commissure of the fornix, forniceal commissure, or the interammonic commissure.[1] Anatomically, the psalterium consists of a triangular space between the two crura of the fornix through which run transverse fibers connecting the crura of the two fornices to each other.[15] The psalterium runs beneath the splenium of the corpus callosum and although is in intimate contact with it, it can be separated and distinguished from it by blunt dissection. Beneath the hippocampal commissure lies the velum interpositum and the roof of the third ventricle.
The vertical group
Internal capsule and the thalamic radiations
The internal capsule is the largest projection fiber system of the brain and consists of five parts, the anterior limb, the genu, the posterior limb, the retrolenticular portion, and the sublenticular portion[1] [Figure 7]. The internal capsule consists of the corticobulbar fibers, the corticospinal fibers, and the thalamic radiations.[1] The corticobulbar and corticospinal tracts lie laterally and the thalamic radiations lie medially. When dissecting from a lateral approach via the insula, one encounters the corticospinal and corticobulbar tracts frst; and, when dissecting from a medial perspective, that is, from the lateral ventricle, the thalamic radiations are revealed first. The anterior limb of the internal capsule lies between the putamen and the head of the caudate nucleus. It consists of the anterior and superior thalamic radiations and the frontopontine fibers.[1] The genu of the internal capsule is the junction of its anterior and posterior limbs and it lies just behind the beginning of the temporal extension of the anterior commissure and in the same coronal plane as the foramen of Monroe.[7] It consists of the superior thalamic radiations, the corticobulbar fibers, and the anterior portion of the corticospinal tract. The posterior limb of the internal capsule lies between the globus pallidus and the thalamus. It consists of the posterior part of the corticospinal tract, the parietal thalamic radiations, and the parietopontine fibers. The retrolenticular portion of the internal capsule includes the parietopontine fibers and some portion of the occipital thalamic radiations. The sublenticular portion of the internal capsule consists of the occipitopontine, the temporopontine, and the major bulk of the occipital thalamic radiation.[1] The anterior bundle of the optic radiations (occipital thalamic and temporal thalamic radiations) lies in the sublenticular portion of the internal capsule; and, the central and posterior bundles lie in the retrolenticular portion of the internal capsule.[1],[13]
External capsule
The external capsule can be divided into two parts: the ventral external capsule and the dorsal external capsule. In the region of the limen insulae, fibers of the external capsule mingle with fibers of the IFOF and the UF to form the ventral portion of the external capsule with the IFOF lying posteriorly and superiorly, and the UF lying anteriorly and inferiorly. These fibers form the ventral portion of the external capsule. The dorsal external capsule is a vertical claustro-cortical projection fiber system that connects the external capsule to the frontal and parietal cortices [Figure 3] and [Figure 4]. It lies between the gray matter of the claustrum laterally and the putamen medially. It courses vertically superiorly beneath the AF and the lateral portion of the superior longitudinal fasciculus to join fibers of the internal capsule to form the corona radiata. The external and internal capsule are capsules of the lentiform capsule on its lateral and medial surface, respectively.
Corona radiata
The external and internal capsule fibers join together at the upper edge of the putamen to form the corona radiata [Figure 3] and [Figure 4]. The corona radiata runs through the majority of the frontal and parietal lobes and bisects the middle group of association fibers into medial and lateral halves.[1] At its medial margin, the callosal fibers join the corona radiata to form the centrum semiovale.
The third layer/deep group
Fornix
Fibers of the fimbria and alveus on the surface of the hippocampus join and then curve superolaterally over the pulvinar of the thalamus to form the crus of the fornix (Latin meaning “vault or arch”) [Figure 9].[1],[5] Further anteriorly, the two crura meet in the midline to form the body of the fornix. The two crura of the fornices are connected to each other by the hippocampal commissure or psalterium. The body of the fornix runs forward to the anterior end of the thalamus, where the fibers of the two sides again separate and arch downward in front of the intraventricular foramen as the columns of the fornix.[1],[5] The fornix constitutes the main efferent pathway from the hippocampus, though it also carries a few afferent fibers.[3] The fibers of the fornix, on approaching the anterior commissure, divide into a pre commissural and a postcommissural portion. The majority of the fibers constitute the postcommissural portion.[15],[16] These fibers arise mainly from the subiculum and terminate into the mammillary body. En route to the mammillary body, the postcommissural fornix also gives fibers to the lateral and anterior nucleus of the thalamus and the lateral septal nuclei. Thus, the anterior nucleus of the thalamus receives fibers from the mamillothalamic tract and also receives direct fibers from the postcommissural fornix. A few fibers pass ventral to the anterior commissure as the precommissural fornix.[5] These fibers originate mainly from the pyramidal cells of the hippocampus. Their input is principally to the septal nuclei, the lateral preoptica area, the anterior part of the hypothalamus, and the nucleus of the diagonal band.[1] The precommisural fibers form a small compact bundle that cannot be detected grossly. The postcommissural fornix terminates into the medial mammillary nucleus.
Mammillothalamic and mammillotegmental tracts
The mammillothalamic tract of Vicqd'Azyr consists of fibers arising from the medial mammillary nucleus. The fibers climb upward to end in the anterior nucleus of the thalamus. Near its origin, the mammillothalamic tract gives rise to another smaller bundle known as the mammillotegmental tract. The mammillotegmental tract runs posteriorly and inferiorly toward the brainstem and then terminates into the tegmental nucleus of Gudden.[5] From the anterior nucleus of the thalamus, fibers of the anterior thalamic radiation diverge upward and mingle with the fibers of the anterior limb of the internal capsule to reach the cingulum (Latin meaning “girdle”) and the cingulate gyrus.[1]
Stria terminalis
The stria terminalis is a C-shaped association fiber that connects the amygdala and the medial forebrain structures. The amygdala gives rise to two major pathways, the stria terminalis, and the ventral amygdalofugal pathway.[5] The stria terminalis runs between the caudate nucleus and the thalamus around the lateral ventricle. The fibers terminate in the bed nuclei of the stria terminalis, which lies lateral to the columns of the fornix and superior to the anterior commissure.[1] Some fibers also terminate in the hypothalamus and some join the medial forebrain bundle.[3] The bed nucleus of the stria terminalis has widespread connections to the rest of the limbic system, and therefore, provides an important route by which the amygdala can affect structures beyond the connections of the stria terminalis itself.
Stria medullaris thalami
This fiber tract runs along the dorsomedial surface of the thalamus in the floor of the lateral ventricle.[1] It runs lateral to the lower lateral edge of the foramen of Monroe near the anterior commissure.[5] It connects the septal area with the habenula.
Clinical implications: Neural networks
Various cortical and subcortical regions connect with each other to perform various functions. Duffau et al. using intra-operative electrical stimulation proposed a probabilistic Atlas More Details of critical hubs and connections subserving some basic human brain functions.[17] Based on our anatomical dissections, we present here briefly the cortical stations and their underlying white matter connections for some of the important activities.[1]
Language and speech
The classical model of language consists of the Broca's area, Wernicke's area, and the AF connecting these two regions. Recently Hickok et al. proposed a dual-stream model for language, the dorsal stream, and the ventral stream.[18]
The ventral stream is involved in processing speech signals for comprehension or speech recognition. The dorsal stream is responsible for translating acoustic speech signals into articulatory representations essential for speech development and speech production. Thus, the dorsal stream is involved with phonological processing and is mediated by the posterior part of the inferior frontal gyrus (pars triangularis and pars opercularis), the posterior portion of the middle forntal gyrus, posterior thirds of the superior and middle temporal gyri, SLF II and III and the AF.[17],[18] The ventral stream of language is involved with semantic processing and is mediated in the dominant hemisphere, the posterior thirds of the superior and middle temporal gyri, the dorsolateral prefrontal cortex, the inferior frontal gyrus, the IFOF, the ILF and the middle longitudinal fasciculus.[17],[18] In the non-dominant hemisphere, this semantic pathway mediates nonverbal comprehension. Stimulation of the most posterior part of the pars opercularis, where it connects with the precentral gyrus, is classically the ventral premotor area, and stimulation in this region in both the hemispheres leads to speech arrest.
Motor/sensory tasks
Traditionally, the precentral gyrus (primary motor cortex) and the corticospinal tracts are the cortical and subcortical substrates of the primary motor system; and, the postcentral gyrus (primary sensory cortex) and the thalamocortical pathways are the cortical-subcortical substrates of the primary somatosensory system. However, both anatomical studies and electrical stimulations have shown that both the systems interact closely and are connected to each other intricately by short intergyral connections.[1],[17],[18]
Motor and speech planning and control
Learning, planning, performing, and control of voluntary movements involve the dorsal medial and lateral pre-motor cortices, the basal ganglia, and their subcortical connections.[17] The cortical substrates involved are the posterior and medial portions of the superior frontal gyrus (supplementary and pre-supplementary motor area), the intersection of the superior frontal sulcus, and the precentral sulcus (dorsolateral pre-motor cortex), the insula, and the basal ganglia.[17] The subcortical network consists of short arcuate fibers that connect these areas, the frontal aslant tract, and the cortico-striatal connections.
Spatial awareness
Spatial awareness and perception are mainly lateralized to the right hemisphere. The anatomical substrates responsible for spatial awareness are the supramarginal gyrus, the posterior portion of the superior temporal gyrus, and the lateral part of the SLF (SLF-II and III).
Vision, reading, and naming
The temporo-parietal-occipital junction is the main anatomical substrate involved in visual semantic processing and damage to the region leads to anomia. The cortical stations are the posterior portion of the superior and middle temporal gyri and the angular gyrus. The white fibers involved are those of the AF, the SLF, the IFOF, the ILF, and the optic radiations, which all intersect at this junction. The primary visual cortex (posterior portion of the calacrine sulcus on its cuneal and lingual surfaces and the optic radiations) subserves vision. The cortical and subcortical substrates involved in reading are the inferior portions of the middle temporal gyrus, the inferior temporal gyrus, the fusiform gyrus, and the ILF in the dominant hemisphere.[17] The cortical areas are also known as the visual word forming area.[17] Damage to the ILF leads to difficulties in reading, face recognition, visual perception, and visual memory.
Auditory perception
The auditory cortex or the Heschl's gyrus with the auditory radiations are the anatomic substrates involved in hearing.
Surgical Implications of the classification
We speculate that the origin of gliomas is from the white matter of the short arcuate fibers, the commissural fibers, and long association fibers in decreasing order of frequency.[2],[3],[19] Despite the fact that gliomas are grouped under the term “malignant” tumors, they have a defined pattern of origin and extension. The extension is disciplined and is along a named white fiber tract and its haphazard extension is restricted or limited by the adjoining traversing tracts. High-grade gliomas follow a similar pattern of tract involvement and confinement related to adjoining traversing tracts. The fibers around the tumor are edematous and the edema is seen to extend along the course of the involved fiber.
Classification of gliomas based on anatomical understanding
Based on our understanding, all gliomas (both low and high grade) could be morphologically classified into two broad categories: localized and diffuse.[2],[3] Localized gliomas arose from the short arcuate fibers of the involved gyrus and were named according to the gyrus they were associated with. The diffuse gliomas arose from the long association fiber bundles or the commissural fibers.[2],[3]
As a general rule, localized gliomas remained confined to the particular gyrus that contained the involved short arcuate fibers. Some gliomas tend to involve the adjacent gyrus through the short arcuate connections between the two neighboring gyri. Gliomas that arose from the long association fibers on either side of the vertical group were confined to the respective side by the vertically coursing projection tracts (vertical group) [Figure 12]. Gliomas that arose medial to the vertical group remained medial to the vertical group and similarly, gliomas that arose lateral to the vertical group remained lateral to it. Gliomas that arose from the commissural fibers had a predilection for bilateral extension. Tumors that arose in the region of the genu and the forceps minor extended bilaterally anteriorly into the medial frontal brain. Tumors of the body of the corpus callosum extended bilaterally into the frontoparietal brain depending on the part of the corpus callosum that was involved. Tumors of the splenium and forceps major extended bilaterally into the medial parieto-occipital lobes. Another peculiarity of the corpus callosal gliomas is that they never crossed the vertical group of fibers and remained confined medial to this group of fibers. | Figure 12: Superior view of tractography images showing the various tracts and its relation to the ventricle. The vertical group of fibers bisects the middle group of fibers into medial and lateral halves. CC: Corpus callosum, FM: Forceps major, T: Tapetum, PF: Projection fibers, Cing: Cingulum, IFOF: Inferior fronto-occipital fasciculus, OR: Optic radiations
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Surgical strategy
Based on this anatomical knowledge and our surgical experience, we discuss novel surgical strategies for glioma resection.[2] We advocate an en-masse surgical resection for both low- and high-grade localized gliomas arising from the short arcuate fibers.[2] A clear plain of dissection was available for most of these gliomas during surgery. This strategy of resection is actually a supra-marginal resection as the glioma is only localized to that region. This kind of resection is possible without using any kind of fluorescence as the complete lesion is removed en masse. This holds true for all localized gliomas except for those in the insula where an en masse resection is difficult due to the presence of the branches of the middle cerebral arteries.
Even tumors that arise from short arcuate fibers in eloquent cortical locations were localized and could be excised by identification of a well-defined plane of resection. The eloquent cortex was seen to be displaced by the growth of the tumor in low-grade tumors and in majority of high-grade tumors. A tailored resection was used for tumors when the eloquent cortex was intra-operatively mapped to be in close vicinity to the tumor. For diffuse tumors from the long tracts, we advocate a safe radical piecemeal excision as a total en masse resection may not be anatomically possible.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
| References | | |
| 1. | Shah A, Goel A, Jhawar SS, Patil A, Rangnekar R, Goel A. Neural circuitry: architecture and function-A fiber dissection study. World Neurosurg 2019;125:e620-38.  |
| 2. | Goel A, Shah A, Vutha R, Dandpat S, Hawaldar A. 'En-masse' tumor resection strategy for low grade gliomas arising from short arcuate fibers-feasibility report on 74 patients treated over 4 years. Neurol India. 2021;69:406-13. |
| 3. | Shah A, Vutha R, Goel A. Radiological evaluation of anatomical extensions of gliomas based on white fiber tracts: Proposal of a novel classification. Neurol India Accepted awaiting publication.[In press] |
| 4. | Klingler J. Erleichterung der makroskopischen Praeparation des Gehirnsdurchden Gefrier prozess. Schweiz Arch Neurol Psychiatry 1935;36:247-56. |
| 5. | Shah A, Jhawar SS, Goel A. Analysis of the anatomy of the Papez circuit and adjoining limbic system by fiber dissection techniques. J Clin Neurosci 2012;19:289-98. |
| 6. | Fernández-Miranda JC, Rhoton AL Jr., Alvarez-Linera J, Kakizawa Y, Choi C, deOliveira EP. Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 2008;62 6 Suppl 3:989-1026. |
| 7. | Fernandez-Miranda JC, Pathak S, Engh J, Jarbo K, Verstynen T, Yeh FC, et al. High-definition fiber tractography of the human brain: Neuroanatomical validation and neurosurgical applications. Neurosurgery 2012;71:430-53. |
| 8. | Yagmurlu K, Vlasak AL, Rhoton AL Jr., Three-dimensional topographic fiber tract anatomy of the cerebrum. Neurosurgery 2015;11 Suppl 2:274-305. |
| 9. | Shah A, Goel A, Patil A, Goel A. Letter to the Editor. Superior longitudinal fasciculus. J Neurosurg 2019;132:1309-11. |
| 10. | Maldonado IL, de Champfleur NM, Velut S, Destrieux C, Zemmoura I, Duffau H. Evidence of a middle longitudinal fasciculus in the human brain from fiber dissection. J Anat 2013;223:38-45. |
| 11. | Kier EL, Staib LH, Davis LM, Bronen RA. MR imaging of the temporal stem: Anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. AJNR Am J Neuroradiol 2004;25:677-91. |
| 12. | Peltier J, Verclytte S, Delmaire C, Pruvo JP, Godefroy O, Le Gars D. Microsurgical anatomy of the temporal stem: Clinical relevance and correlations with diffusion tensor imaging fiber tracking. J Neurosurg 2010;112:1033-8. |
| 13. | Shah A, Jhawar SS, Goel A. Letter to the Editor: Optic radiations and anterior commissure. J Neurosurg 2015;123:824-6. |
| 14. | Goel A, Shah A, Ramdasi R, Patni N. Orbital cortical approach to lesions around the frontal horn of the lateral ventricle: Indication and surgical parameters. Acta Neurochir (Wien) 2014;156:825-30. |
| 15. | Ribas GC. The cerebral sulci and gyri. Neurosurg Focus 2010;28:E2. |
| 16. | Wen HT, Rhoton AL Jr, de Oliveira E, Cardoso AC, Tedeschi H, Baccanelli M, et al. Microsurgical anatomy of the temporal lobe: Part 1: Mesial temporal lobe anatomy and its vascular relationships as applied to amygdalohippocampectomy. Neurosurgery 1999;45:549-91. |
| 17. | Sarubbo S, Tate M, De Benedictis A, Merler S, Moritz-Gasser S, Herbet G, et al. Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: An original functional atlas of the human brain. Neuroimage 2020;205:116237. |
| 18. | Hickok G, Poeppel D. Towards a functional neuroanatomy of speech perception. Trends Cogn Sci 2000;4:131-8. |
| 19. | Goel A, Shah A, Dandpat S, Rai S, Prasad A. Gliomas are 'confined' to a named white matter tract: A revolution in understanding gliomas. J Craniovert J Spine 2020;1:252-3. |
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12]
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