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GENERAL Surgical Anatomy and Technique

Microsurgical Anatomy of the and Related Fibers in 3-Dimensional Images

Richard Gonzalo Pa´rraga, BACKGROUND: The fiber dissection technique provides unique 3-dimensional ana- MD* tomic knowledge of the . Guilherme Carvalhal Ribas, OBJECTIVE: To examine the optic radiation anatomy and its important relationship MD‡§ with the temporal stem and to discuss its findings in relation to the approaches to k Leonardo Christiaan Welling, lesions. MD* METHODS: We studied 40 cerebral hemispheres of 20 brains that had been fixed in formalin solution for 40 days. After removal of the arachnoid membrane, the hemi- Raphael Vicente Alves, MD* spheres were frozen, and the Klingler technique was used for dissection under mag- Evandro de Oliveira, MD, nification. Stereoscopic 3-dimensional images of the dissection were obtained for PhD*§¶ illustration.

*Institute of Neurological Sciences, RESULTS: The optic radiations are located deep within the superior and middle tem- Microneurosurgery Laboratory, Benefi- poral gyri, always above the inferior temporal sulcus. The mean distance between the ceˆncia Portuguesa Hospital, Sa˜oPaulo, cortical surface and the lateral edge of the optic radiation was 21 mm. Its fibers are SP, Brazil; ‡Department of Surgery-LIM 02, University of Sa˜o Paulo Medical divided into 3 bundles after their origin. The mean distance between the anterior tip of School, Sa˜o Paulo, SP, Brazil; §Micro- the temporal horn and the Meyer loop was 4.5 mm, between the temporal pole and the neurosurgery Laboratory, Beneficeˆncia anterior border of the Meyer loop was 28.4 mm, and between the limen insulae and the Portuguesa Hospital, Sa˜o Paulo, SP, Brazil; Institute of Neurological Sciences, Meyer loop was 10.7 mm. The mean distance between the lateral geniculate body and k Neurosurgeon Hospital Israelita Albert the lateral margin of the central bundle of the optic radiation was 17.4 mm. Einstein, Sa˜o Paulo, SP, Brazil; ¶Depart- CONCLUSION: The white matter fiber dissection reveals the tridimensional intrinsic ment of Neurosurgery, State University of Campinas-UNICAMP, Campinas, SP, Brazil architecture of the brain, and its knowledge regarding the temporal lobe is particularly important for the neurosurgeon, mostly because of the complexity of the optic radia- Correspondence: tion and related fibers. Evandro de Oliveira, MD, PhD, Instituto de Cieˆncias Neurolo´gicas, KEY WORDS: Fiber dissection, Microsurgical anatomy, Optic radiation, Sagittal stratum, Surgical approaches, Prac¸a Amadeu Amaral, Temporal stem, Visual deficits 27, 5 Andar, CEP 01327-010, Sa˜o Paulo, SP, Brazil. Neurosurgery 71[ONS Suppl 1]:ons160–ons172, 2012 DOI: 10.1227/NEU.0b013e3182556fde E-mail: [email protected]

Received, August 15, 2011. emporal lobe surgery has been developed fibers, facilitating the dissection of the fiber tracts. Accepted, November 30, 2011. further over the years, particularly as a result The temporal lobe and the optic radiation anatomy Published Online, March 26, 2012. of the development of microsurgical tech- are illustrated with 3-dimensional stereoscopic T 12-16 niques, magnetic resonance images, and new brain anaglyphic images. Copyright ª 2012 by the 1-6 Congress of Neurological Surgeons mapping techniques. The intrinsic brain structure is composed of MATERIALS AND METHODS myelinized fibers that are collected together in 3 basic types of fascicles or tracts: The association Forty normal brain hemispheres were fixed in fibers connect the different cortical areas in the formalin for at least 40 days,8,10 and then the arachnoid same hemisphere; the commissural fibers connect membrane and vessels were removed under the both hemispheres; and the projection fibers link magnification (6·-40·) provided by a M900 D.F. the different brain areas to the brainstem and to the Vasconcellos microscope (D.F Vasconcellos SA, São Paulo, SP, Brazil). The hemispheres were frozen at spinal cord.7-10 Diffusion tensor images can 215°C for at least 14 days, and dissections were done provide the delineation of these fibers and their 11 with wooden spatulas of different sizes. The dissection relations with intra-axial and extra-axial lesions. started at the lateral temporal surface as described This study was performed according to the by Türe et al,10 and the basal surface was dissected 8,9 Klingler dissection technique because the water up to the floor of the temporal horn. Ultimately, expansion resulting from freezing spreads the the dissection continued after the removal of the

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ependymal layer to identify the optic radiation origin along the pulvinar Stereoscopic images were obtained12-14,19,20 with a Nikon D40 and lateral geniculate body and along their course up to the superior and camera and the following lenses: AF-S Nikkor 18 to 55 mm 1:3.5 to inferior edges of the calcarine fissure. Furthermore, the Meyer loop, the 5.6 GII ED and AF-S VR Micro-Nikkor 105 mm f/2.8 G (Nikon Corp, , the anterior commissure, and other structures related to the Sendai, Japan). The callipygian software was used to develop the temporal stem were also identified and dissected (Figure 1).8,10,15-18 anaglyphic images (Callipyan 3D; © 2003, Robert Swirsky), and the It is not always possible to separate the different fiber systems from statistical analysis of the findings was performed with SPSS 15.0 software each other and, in particular, to always obtain a reliable anatomic (SPSS Inc, Chicago, Illinois). differentiation within the so-called sagittal stratum,9,10 despite the use of meticulous dissection microtechniques. For instance, exposure of a given fiber tract often results in the destruction of another one. RESULTS The following measurements were done: (1) the optic tract length and The Optic Tract diameter, (2) the distance between the tip of the Meyer loop and the temporal pole, (3) the distance between the anterior tip of the temporal The optic tract follows a posterolateral trajectory after leaving horn and the anterior edge of the Meyer loop, (4) the distance between the optic toward the external border of the . Its the lateral geniculate body and the anterior edge of the Meyer loop, (5) the average length was 30.7 mm. The anterior half-diameter was 3.7 distance from the cortical surface to the optic radiation lateral edge at the mm and the posterior half-diameter was 5.5 mm. The majority of level of the geniculate lateral body, and (6) the length of the lateral aspect its fibers reached the lateral geniculate body, which is a small ovoid of the optic radiation (Figure 1). mass located under the pulvinar of the thalamus and anterolateral to the medial geniculate body. A minority of fibers were found reaching the pulvinar, the pretectal nucleus, and the superior colliculi (Figure 2).

The Optic Radiations The optic radiation fibers are constituted by from neurons of the lateral geniculate body and from the pulvinar of the thalamus that reach the calcarine cortex (Brodmann area 17) within the superior and inferior lips of the calcarine fissure. Each optic radiation is composed of fibers from the temporal ipsilateral and the nasal contralateral retinal halves. Its average length was 95 mm. It constitutes part of the posterior thalamic peduncle; passes under the lentiform nucleus as fibers of the sublenticular part of the , above the and the tail of the ; and joins the sagittal stratum that forms the lateral ventricular wall. The optic radiation fibers can be divided into 3 portions after its origin: the anterior bundle, the central bundle, and the posterior bundle.21

The Anterior Bundle (Meyer Loop) After its origin, the fibers that constitute the anterior bundle follow an anterolateral direction along the roof of the temporal horn, lateral to the amygdala and perpendicular to the anterior commis- sure. The distance from the ambient gyrus (uncus) to the Meyer loop was 22 mm (Figure 3). Anterior to the temporal horn, the fibers shift backward, characterizing the Meyer loop, assuming a postero- lateral course, hence becoming lateral to the temporal horn and to the atrium, and ending along the inferior lip of the calcarine fissure. FIGURE 1. Inferior view of the optic radiation with the measurements that were The distance between the temporal pole and the anterior edge of done. A-B, the distance between temporal pole (TePo) and the anterior edge of the Meyer loop. C-D, distance between the anterior wall of temporal horn and the the Meyer loop was 28.4 mm (20-33 mm). The anterior border anterior edge of the Meyer loop. E-F, distance between the anterior edge of was about 4.5 mm (2-7 mm) anterior to the temporal horn in all the Meyer loop and the lateral geniculate body (LatGeBo). G-H, distance specimens. At this level, the anterior commissure fibers were found between the lateral geniculate body and the lateral edge of the optic radiation. I-J, to be intermingled with the optic radiation fibers. distance between the cortical surface of the middle temporal gyrus and lateral edge The distance between the limen insulae and the Meyer loop or of the optic radiation. K-L, length of the optic radiation. AntB, anterior bundle; anterior bundle was 10.7 mm (7-13 mm). The average length from Atr, atrium of lateral ventricle; CenB, central bundle; HippoHead, head of the ; PostB, posterior bundle. the anterior edge of the Meyer loop and the lateral geniculate body was 21 mm (18-28 mm).

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FIGURE 2. Images in 3 (A) and 2 (B) dimensions. Inferolateral view of the FIGURE 3. Images in 3 (A) and 2 (B) dimensions. View of the roof of the left right hemisphere. The lenticular nucleus, anterior commissure (AntCom), occi- temporal horn, where the ependyma, tapetum, and choroid plexus have been pitofrontal, superior longitudinal (SupLongFasc), and uncinate fascicles have partially removed to disclose the origin and trajectory of the bundles of optic been partially removed to expose the corona radiate (CoRa), internal capsule, radiation (OptRad). The anterior bundle (AntB; red), central bundle (CenB; optic radiation (OptRad), and optic tract (OptTr). AntLimb, anterior limb of the yellow), and posterior bundle (PostB; green) are shown. LatGeBo, lateral internal capsule; CoFo, column or pillar of the fornix; CoStrFi, cortical striatal geniculate body; MeGeBod, medial geniculate body; OptTr, optic tract; Pulv, fibers; MaBo, ; Put, . pulvinar of thalamus; UncFasc, uncinate fasciculus.

Relationships of the Optic Radiation With the Temporal The Central Bundle Sulci and Gyri at the Lateral Surface The central bundle initially follows a lateral direction crossing The optic radiation is located within the depth of the middle superiorly the roof of the temporal horn and then turns sharply, and superior temporal gyri, always above the level of the inferior following a posterior course lateral to the atrium and to the temporal sulcus (Figure 6). The mean distance between the occipital horn, passing above and through the inferior longitudinal cortical surface of the middle temporal gyrus and the lateral edge fasciculus, and ending at the lateral aspect of the occipital pole. Its of the optic radiation was 21 mm. anterior third covers the auditory radiation, and below the central bundle lies the tapetum medially, which is separated from the ventricular cavity only by the ependymal layer (Figures 4 and 5). Relationships With the Temporal Stem and The distance between the lateral geniculate body and the central Sagittal Stratum bundle was 17.4 mm. Laterally, the parahippocampal gyrus is contiguous with the fusiform gyrus and with the remainder of the basal surface of the The Posterior Bundle brain. Posteriorly, it continues along the cingulate gyrus. Medially, The posterior bundle courses posteriorly, forming the lateral it runs under the thalamus along the natural space comprising wall and part of the roof of the atrium and occipital horn, ending the perimesencephalic cistern.22 Anteriorly, its uncal portion is along the superior lip of the calcarine fissure (Figures 4 and 5). superiorly incorporated into the lateral most aspect of the

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FIGURE 4. Images in 3 (A) and 2 (B) dimensions. Lateral view. Optic FIGURE 5. Images in 3 (A) and 2 (B) dimensions. Magnified view of the radiation (OptRad) of the left hemisphere; the section of the superior longitudinal trajectory of the central and posterior bundles. The tapetum constitutes the fasciculus (SupLongFasc) allows exposure of the central (CenB) and posterior medial roof of the ventricular atrium. CenB, central bundle; OptRad, optic bundles (PostB), which end at the lateral aspect of occipital pole and superior lip radiation; PostB, posterior bundle; SupLipCaF, superior lip of the calcarine of the calcarine fissure, respectively. AntCom, anterior commissure; CaN, caudate fissure; SupLongFasc, superior longitudinal fasciculus; Spl, splenium of the nucleus; CoRa, ; DiBandBr, ; GloPa, corpus callosum. ; IntCap, internal capsule.

frontobasal region via a well-defined neural peduncle anterior to Posterolaterally, this temporal peduncle is contiguous with the the inferior horn of the lateral ventricle. layers of fibers called the sagittal stratum,9,10 which covers the Anteriorly and externally, this true temporal peduncle is com- inferior horn and ventricular atrium. All of these structures posed of the cortex of the transverse insular gyrus, which crosses the collectively join the temporal lobe to the remainder of the cerebral limen insulae, connecting the to the posteromedial hemisphere beneath the insula. The so-called sagittal stratum orbitallobule.23 Internally, it consists of the uncinate fascicle (which consists of the fronto-occipital fascicle, the posterior thalamic joins the frontal and temporal lobes),24 occipitofrontal fasciculus peduncle (which contains the optic radiation), and the fibers that (which are located immediately posterior to the uncinate fascicle; compose the anterior commissure. The layer of callosal fibers Figure 7), amygdalofugal fibers (which are composed of the ventral known as the tapetum lies under the optic radiation and then extensions of the amygdala that project to the septothalamohypo- constitutes the layer that is immediately underneath the sagittal thalamic region),25 nucleus of the stria terminalis (situated under stratum (Figures 8 and 9). The sagittal stratum is situated inferior the head of the caudate nucleus),26-28 and fibers of the anterior to the inferior limiting sulcus of the insula, forming the roof and commissure. Medially, there is the superior extension of the lateral wall of the inferior horn, and also constitutes the lateral amygdala, which forms the anterior half of the uncus and extends wall of the ventricular atrium (Figure 8). Superficial to the sagittal posteriorly over the head of the hippocampus and then superiorly stratum is the subcortical white matter of the entire neocortical and medially toward the globus pallidus.29 portion of the temporal lobe.

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FIGURE 6. Images in 3 (A) and 2 (B) dimensions. Lateral view. The superior, FIGURE 7. Images in 3 (A) and 2 (B) dimensions. Lateral view of left middle temporal, angular, and occipital gyri were removed. Observe the optic hemisphere. Parts of the superior longitudinal fasciculus (SupLongFasc) were radiation located deep to the superior and middle temporal gyri, above the inferior removed to expose the corona radiata and the sagittal stratum (SagStr). Occi- temporal sulcus. CS, central sulcus; Inf. Temp. Sulcus, inferior temporal sulcus; pitofrontal (OcFrFasc) and uncinate fasciculus (UncFasc) can be identified InfLimS, inferior limiting sulcus; ITG, inferior temporal gyrus; MFG, middle passing along the basal portion of the insular cortex. AntCom, anterior com- frontal gyrus; OptRad, optic radiation; PostCG, postcentral gyrus; PreCG, missure; CoRa, corona radiate; GloPa, globus pallidus. precentral gyrus; SPLob, superior ; TePo, temporal pole.

extension passes along the basal portion of the globus pallidus, Relationships With the Other Fascicles perpendicular to the optic radiation and medial to the uncinate The optic radiation is also related with other also important fascicles fascicle. Some fibers of the lateral extension anteriorly reach the within the white matter: the anterior commissure, the acustic radiation, uncinate fascicle and the temporal pole, but most of its fibers and the uncinate, occipitofrontal, and superior longitudinal fascicles. follow a posterior direction, joining the occipitofrontal fascicle and becoming part of the sagittal stratum.10,18,31 The lateral The Anterior Commissure extension of the anterior commissure covers the anterior and The anterior commissure is made up of fibers that connect the central bundles of the optic radiation, and when it reaches the anterior and mesial aspects of both temporal lobes. It forms dorsal aspect of the temporal lobe, the anterior commissure fibers a compact, round bundle structure at the midline and extends become diffusely spread like a fan (Figure 10). The fibers of the laterally, somewhat like the handlebars of a bicycle. It crosses in anterior commissure are superior and also partially intermingled front of the fornix columns (some fibers of the fornix pass with the fibers of the optic radiation. The exposure of the optic anteriorly to the anterior commissure toward the septal nuclei) radiation then requires the removal of the most superior fibers of and extends laterally along the temporal stem, posteriorly to the the anterior commissure (Figure 11). uncinate fascicle, and anteriorly and superiorly to the temporal horn of the lateral ventricle, fanning into the temporal gyri. Acustic Radiations Bilateral anterior extensions (anterior crus) connect both olfactory The acustic fibers course through the sublenticular portion of systems, creating a real olfactive commissure.22,25,30,31 The lateral the internal capsule and end along the transverse temporal gyri

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FIGURE 8. Images in 3 (A) and 2 (B) dimensions. Lateral view of the left FIGURE 9. Images in 3 (A) and 2 (B) dimensions. Medial view of the left hemisphere. The vertical segment of the superior longitudinal fasciculus hemisphere. The ependyma of the lateral ventricle and left atrium was removed. (SupLongFasc) was removed, and a window in the sagittal stratum (SagStr) was Note the relation of the tapetum with the thalamic peduncles. The tapetum lies created to expose the tapetum. CoRa, corona radiata; ExtCap, ; underneath the optic radiation along the lateral wall of the atrium. AntCom, ExtrCap, ; LoG, long gyri of insula. anterior commissure; CN III, cranial nerve III; Corp. Call., corpus callosum; MaBo, mammillary body; Sub. Nucl., .

(Heschl gyrus). They are related superiorly to the temporal horn, Occipitofrontal Fasciculus the atrium, the optic radiation, and the anterior commissure 25,31 The occipitofrontal fasciculus is a large association bundle of (Figure 8). fibers that connects the frontal and occipital lobes. It passes along the basal portion of the insula and the , immediately above Uncinate Fascicle the uncinate fascicle (Figure 7), and there was no defined limit The uncinate fasciculus, which has its name because of its between the occipitofrontal and the uncinate fascicles, with their hooklike shape, is approximately 2 mm thick at the level of the limen merging in the extreme and external capsules.10,24,31,34 It coursed insulae (Figure 7).24 Its posterosuperior margin is adherent to the parallel to and above the optic radiation in all specimens. occipitofrontal fascicle just under the putamen and the claustrum. The uncinate fascicle joins the temporal stem and lies under the Superior Longitudinal Fasciculus cortex of the limen insulae (anterior transverse gyrus of the The superior longitudinal fasciculus, or arcuate fascicle, is a large insula)10 and anterior to the Meyer loop, anterior commissure, association bundle located around the sylvian fissure and the occipitofrontal fasciculus, and inferior thalamic peduncle. It mostly insula, which connects the frontal, parietal, temporal, and occipital connects the anterior and medial aspects of the temporal lobe with lobes. Along its temporal course, it covers the sagittal stratum the orbital portion of the .17,24,31-33 The uncinate (Figure 7), which includes the optic radiation fibers, the anterior fasciculus was found to be anterior to the optic radiation anterior commissure, and the occipitofrontal bundle. The superior bundle (the Meyer loop) in all specimens. longitudinal fasciculus can be followed along the wall of the

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FIGURE 11. Images in 3 (A) and 2 (B) dimensions. Magnified lateral view. The internal capsule was partially removed to expose the head and body of the caudate nucleus. The portion of the ventricular frontal horn anterior to the head of the caudate can be appreciated. AntCom, anterior commissure; CaN, caudate nucleus; CoRa, corona radiata; DiBandBr, diagonal band of Broca; GloPa, globus pallidus; IntCap, internal capsule; NuclAccumb, ; OptRad, optic radiation; SepPel, septum pellucidum; SupLongFasc, superior longitudinal fasciculus.

FIGURE 10. Images in 3 (A) and 2 (B) dimensions. Anterolateral view of the left hemisphere. The occipitofrontal and the uncinate fasciculi and the putamen Inferior Longitudinal Fasciculus were removed to expose the anterior commissure. The diagonal band of Broca (DiBandBr) and its junction with the amygdala are inferior to the lateral aspect This fasciculus extends from the to the temporal 22,25 of the anterior commissure (AntCom). CoRa, corona radiata; GloPa, globus pole, within the depth of the fusiform gyrus. It was found that pallidus; HippoHead, head of the hippocampus; IntCap, internal capsule; SagStr, along its course the inferior longitudinal fasciculus lies inferior sagittal stratum; SupLongFasc, superior longitudinal fasciculus. and lateral to the optical radiations and inferior and parallel to the temporal horn. lateral ventricle, within the depth of the middle frontal and the inferior parietal and middle temporal gyri, encircling the insula in a “C” shape (Figure 12).10,22,31 Two segments can be identified Relationships With the Ventricles according to their fiber orientation: the horizontal segment in the In all the hemispheres studied, the optic radiation covered the depth of the middle frontal gyrus and inferior parietal lobule and roof and the lateral wall of the temporal horn, atrium, and occipital a vertical segment that runs along the posterior portion of the horn and the floor of the atrium and occipital horn. The anterior inferior parietal lobule and the superior and middle temporal border of the Meyer loop was always anterior to the tip of the gyri.15 It is important to highlight that the vertical segment always temporal horn. The medial walls of these ventricular compart- covers the sagittal stratum and therefore the optic radiation. ments were not related to the optic radiation except at the level of

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white matter dissection refinement provided by Klingler in 1935 (Figure 13).8-10,35 The individual features of the optic radiation cannot be defined precisely by use of the fiber dissection technique because of the dense network between its fibers and the fibers of the uncinate fascicle, occipitofrontal fasciculus, anterior commissure, inferior thalamic peduncle (which contains the amygdalothalamic fibers), posterior thalamic peduncle (which contains the optic radiation), tempor- opontine, and occipitopontine, particularly in the area of the so-called sagittal stratum.10 In addition, the dissection and exposure of each fiber tract often result in the destruction of other fiber tracts.35 However, the major bulk of the optic radiation was always identified and dissected in all our specimens, corroborating its division in anterior, central, and posterior bundles as previously described by Ebeling and Reulen.21 The Meyer loop is formed by the anterior bundle of the optic radiation fibers that are directed forward from the lateral geniculate body toward to the temporal pole and located anterior to and around the tip of the temporal horn roof in the lateral ventricle. It is the most vulnerable part of the optic radiation in terms of the approaches to the temporal horn and the temporomedial region. Damage to this anterior bundle often results in superior homonymous quadranta- nopic deficits,21,37-39 and it occurs in 50% to 90% of cases after anterior temporal lobectomies.40 The exact fiber course of the Meyer loop is controversial. Some authors describe these fibers as also being anterior to the temporal horn tip36,41,42; others indicate that these fibers reach only the level of the temporal horn tip.43-45 The most anterior limit of the Meyer loop has also been at the center of debate; it is estimated to FIGURE 12. Images in 3 (A) and 2 (B) dimensions. Lateral view of left be anywhere from 22 to 37 mm posterior to the temporal hemisphere. The vertical segment of the superior longitudinal fasciculus pole.16,21 Penfield46 noticed that lesions , 60 mm from the (SupLongFasc) has been removed to expose the optic radiation (OptRad). temporal tip were not likely to produce a field defect. Falconer AntCom, anterior commissure; CoRa, corona radiata; GloPa, globus pallidus; and Wilson47 suggested that the Meyer loop anterior limit IntCap, internal capsule; POS, parieto-occipital sulcus; PreCu, precuneus; Cu, . location is about 45 mm from the temporal pole tip. Bjork and Kugelberg43 estimated the anterior limit to be between 30 and 40 mm. Marino and Rasmussen43 reduced the safely resected area the lateral geniculate body. The floor of the temporal horn was also length and reported that the smallest defect occurred with not related to the optic radiation. a resection of 40 mm. The anterior edge of the Meyer loop was 28.4 mm (20-33 mm) from the temporal pole in our study. DISCUSSION Ebeling and Reulen21 described the Meyer loop as being located from 10 mm ahead to 5 mm behind the temporal horn The Optic Radiation and Its Main Relationships tip. We observed in our study that the fibers extended ahead of The origin, course, and termination of the optic radiation were the temporal horn tip in all specimens (average, 4.5 mm). dissected and described for the first time by the great French Sincoff et al48 found that the optic radiation inferior edge is neuroanatomist (1815-1865); it received its never below the inferior temporal sulcus. These authors described name in 1854.10,35 The Italian anatomist Bartholomeo Panizza the lateral wall and temporal horn tip and roof as being (1785-1867) demonstrated the visual pathway from the eye to the completely covered by the optic radiation and the floor and occipital cortex using the fiber dissection technique in 1855.10 medial wall of the temporal horn as being free from the optic The first description of the optic radiation course within the radiation, except the level of the lateral geniculate body, similar to temporal lobe with its anterior fibers going anteriorly and then our findings (Figure 14A). curving posteriorly was provided by Flechsig in 1896, who called Regarding the so-called temporal stem, although controver- it the temporal knee,35 and posteriorly in 1907 by Meyer,36 who sial,35 a well-defined neural peduncle constituted by the uncinate called it the temporal loop. The relationships between the optic fasciculus fibers of the occipitofrontal fasciculus, amygdalofugal radiation and its more related structures became clearer with the fibers, and fibers of the anterior commissure can always be

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FIGURE 13. Images in 3 (A) and 2 (B) dimensions. Basal view of the neural visual pathways. The temporal gyrus has been removed bilaterally, preserving the optic radiations (OptRad). The temporal stem has been removed, exposing the Meyer loop and the trajectory of its fibers that reach the inferior lip of the calcarine fissure (InfLipCaF). In the left temporal horn, the ependyma has been removed, and the tapetum can be seen along the atrium. AntCom, anterior commissure; AntLimb, anterior limb of the internal capsule; LatGeBo, lateral geniculate body; OpCh, optic chiasm; OptTr, optic tract; PreCu, precuneus; UncFasc, uncinate fasciculus. identified anterior to sagittal stratum, connecting the mesial From a topographical perspective, it is notable that the sagittal aspect of the temporal lobe with the basal . stratum corresponds to the set of fibers that cover the inferior horn In the literature, this set of structures has been given the generic and atrium of the ventricle, inferior and posterior to the insula, and controversial name of temporal stem described in different whereas the temporal stem is situated anterior to the inferior horn, ways. According to Duvernoy,49 “the temporal stem consists of connecting the anteromedial temporal portion to the basolateral only a thin layer of white matter situated between the ventricular frontal portion of the brain. cavity and the fundus of the superior temporal sulcus.” Wen According to this concept and our findings, the so-called et al29 stated that the term refers “only to the connections temporal stem itself lies medially and anteriorly to the optic between the temporal lobe and the insula, excluding the superior radiation, and the sagittal stratum contains the temporal portion of extension of the amygdala in the direction of the globus pallidus the optic radiation. and the limen insulae.” Tuüre et al50 defined the temporal stem as “the portion of white matter that penetrates the temporal lobe Considerations Regarding Approaches to the between the anterior border of the insula and the inferior horn, Temporal Horn composed of the fronto-occipital fascicle and the anterior There are many microneurosurgical corridors toward the thalamic peduncle.” We agree with this assessment because this inferior or temporal horn that were usually developed primarily true temporal peduncle constitutes a very well-defined anatomic for the surgical treatment of temporal lobe epilepsy. They are all feature that distinguishes the temporal lobe from the other based on the initial description of the transtemporal transven- morphologically similar white matter connections between the tricular removal of the amygdala and of the hippocampus by cerebral lobes, including the other connections of the temporal Niemeyer51 in 1958 and currently can be divided into 3 groups lobe itself. of approaches: transsylvian, lateral, and subtemporal approaches.

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commissure, occipitofrontal fasciculus, and potentially the anterior aspect of the Meyer loop (Figure 14B). Vajkoczy et al54 proposed the transsylvian-transcisternal for the en bloc resection of the mesial structures, particularly for the treatment of patients with . With this technique, the anterior hippocampus and the amygdala are resected “en bloc” through the division of the rhinal sulcus, with the preservation of the laterobasal surface integrity of the temporal lobe. Coppens et al55 described the transsylvian anteromedial approach to access the temporal horn, through a small incision in the pyriform cortex, to reach the amygdala medially to the uncinate fascicle, limen insulae, and optic radiation. Choi et al56 identified a triangular area under the sylvian fissure floor to reach the temporal horn, medial to the Meyer loop and lateral to the optic tract. Its base is formed by the limen insulae level and its apex by the anterior border of the lateral geniculate body; the amygdala was located in the anterior portion of this triangle. Lateral Transtemporal Approaches Through the Superior, Middle, or Inferior Temporal Gyrus The lateral approaches when done through the middle temporal gyrus can lead to contralateral quadrantanopia (Figure 14B). The lateral wall of the temporal horn is located 22 to 26 mm from the cortical surface at this level, and visual deficit occurred in about 7% of the patients submitted to this technique.21,24,31 It is also important to consider that in the dominant hemisphere the middle temporal gyrus has connections with the angular gyrus, which, together with the parietal and the occipital lobes, plays an important functional language role. Olivier57 described in 1991 the transsulcal approach through the superior temporal sulcus, which also implies possible visual deficits and language impair- ments because the language areas can extend along the dominant superior temporal gyrus until 5 to 6 cm behind the temporal pole.4 The approach to the inferior horn through the inferior temporal gyrus can be made 3 cm posterior to the temporal pole and avoids damage to the visual and language pathways,58 also according to FIGURE 14. A, illustration showing a summary of the optic radiation our findings. relations with the sulci, gyri, and lateral ventricle. The anterior bundle (red), central bundle (yellow), and posterior bundle (green). CaF, calcarine fissure; Subtemporal Approaches Through the Uncus and Inf. Temp. Sulcus, inferior temporal sulcus; ITG, inferior temporal gyrus; Parahippocampal Gyrus and Through the Fusiform Gyrus MTG, middle temporal gyrus; STG, superior temporal gyrus; Sup. Temp. Park et al59 described the subtemporal transparahippocampal Sulcus, superior temporal sulcus; TeHo, temporal horn. B,photographshowing a left in 3 dimensions. The exposure gained through approach to perform amygdalohippocampectomies (Figure 14B). approaches to the temporal horn and trigone. Pterional/transsylvian, trans- A cortical incision is made in the uncus, 1 to 1.5 cm posterior to ventricular approaches (red), transtemporal and subtemporal approaches the point where the third nerve crosses the tentorial edge for the (yellow), supracerebellar transtentorial approach (green), and parieto-occipital exposure of the temporal horn, and the anterior hippocampus is interhemispheric approach (blue). removed subpially. They reported an operative morbidity consisting of a contralateral homonymous quadrant visual defect in 1 patient and memory impairment in 1 patients among 8 patients. In 1993, Hori et al60 proposed a similar approach Transsylvian Transventricular through the fusiform gyrus for the treatment of temporal lobe The transsylvian transventricular approach proposed by epilepsy with some modifications such as dividing the tentorium Yas¸argil and colleagues37,52,53 along or just lateral to the limen in an effort to reduce retraction on the temporal lobe, emphasized insulae and to the inferior limiting sulcus avoids damage to the measures to avoid damage to the vein of Labbé, and advocated the dorsal cortical surface but damages the uncinate fascicle, anterior en bloc excision of the fusiform gyrus to open the temporal horn.

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According to Yeni et al,61 the incidence of the superior 2. Berger MS. Functional mapping-guided resection of low-grade gliomas. Clin quadrantanopia is 50 to 90% after an anterior temporal lobectomy. Neurosurg. 1995;42:437-452. 3. Lehéricy S, Duffau H, Cornu P, et al. Correspondence between functional Renowden et al reported 50% of incomplete quadrantanopia after magnetic resonance imaging somatotopy and individual brain anatomy of the selective amygdalohippocampectomies, in contrast to the Yas¸argil central region: comparison with intraoperative stimulation in patients with brain et al62 series in which only 1 of 73 patients developed a visual tumors. J Neurosurg. 2000;92(4):589-598. deficit after transsylvian selective amygdalohippocampectomies. 4. Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere: an electrical stimulation mapping investigation in 117 The temporal horn and atrium may also be reached through the patients. J Neurosurg. 1989;71(3):316-326. supracerebellar transtentorial approach, thus avoiding lesions of 5. Ruge MI, Victor J, Hosain S, et al. Concordance between functional magnetic the optic radiation (Figure 14B). resonance imaging and intraoperative language mapping. Stereotact Funct Neuro- surg. 1999;72(2-4):95-102. 6. Schiffbauer H, Berger MS, Ferrari P, Freudenstein D, Rowley HA, Roberts TP. Considerations Regarding Approaches to the Trigone Preoperative magnetic source imaging for brain tumor surgery: a quantitative Fornari et al63 proposed a parietal transcortical approach to the comparison with intraoperative sensory and motor mapping. J Neurosurg. 2002;97 trigone through the superior parietal gyrus. According to these (6):1333-1342. 7. Meynert TH. Vom Gehirne der Saugethiere. In: Stricker, ed. Handbuck der Lehre authors, such parieto-occipital approaches are not the cause of visual von Geweben des Menschen und der Thiere. Vol II. Leipzig, Germany: Engelmann; damage because the optic radiation lies more inferolateral to the 1872:694-808. Cited by: Türe U, Yas¸argil MG, Friedman AH, Al-Mefty O. Fiber ventricle. A similar approach was proposed by Ribas et al64 through dissection technique: lateral aspect of the brain. Neurosurgery. 2000;47(2): the opening of the intraparietal sulcus started anteriorly at the 417-427. 8. Klingler J. Development of the macroscopic preparation of the brain through the meeting point of the postcentral and intraparietal sulci, because this process of freezing [in German]. Schweiz Arch Neurol Psychiatr. 1935;36:247-256. meeting point has a very close relationship with the ventricular 9. Ludwig E, Klingler J. Atlas Cerebri Humani. Basel, Switzerland: S. Karger; 1956. trigone and can easily be found underneath the skull about 6 cm 10. Türe U, Yas¸argil MG, Friedman AH, Al-Mefty O. Fiber dissection technique: anterior to lambda and 5 cm lateral to the sagittal suture. lateral aspect of the brain. Neurosurgery. 2000;47(2):417-427. 65 11. Witwer BP, Moftakhar R, Hasan KM, et al. Diffusion-tensor imaging of white Nagata andSasaki described a lateral transsulcal approach to the matter tracts in patients with cerebral neoplasm. J Neurosurg. 2002;97(3):568-575. atrium through a horizontal cortical incision made at the posterior 12. Párraga RG, Ribas GC, Andrade SE, de Oliveira E. Microsurgical anatomy of the aspect of the insular cortex. For these authors, the advantages of posterior cerebral artery in three-dimensional images. World Neurosurg. 2011;75 (2):233-257. such a lateral transsulcal approach are a direct and wide operative 13. Ribas GC, Bento RF, Rodrigues AJ Jr. Anaglyphic three-dimensional stereoscopic field, the use of a definite anatomic landmark, easy exposure of the printing: revival of an old method for anatomical and surgical teaching and choroid plexus, and no damage to the optic radiation. reporting. J Neurosurg. 2001;95(6):1057-1066. The parieto-occipital interhemispheric approach was described 14. Ribas GC, Ribas EC, Rodrigues AJ Jr. The brain, the tridimensional vision, and 66,67 the techniques to obtain stereoscopic images. Rev Med (Sao Paulo). 2006;85:78-90. by Yas¸argil and colleagues. Through a large exposure of the 15. Fernández-Miranda F, Rhoton AL, Álvarez-Linera J. Three-dimensional micro- parasplenial area, the trigone can be approached through a small surgical and tractographic anatomy of the white matter of the . cortical incision made just anterior to the parieto-occipital sulcus Neurosurgery. 2008;62(6 suppl 3):989-1027. (Figure 14B). Rhoton30 described the same approach, although 16. Rubino PA, Rhoton AL Jr, Tong X, Oliveira E. Three-dimensional relationships of the optic radiation. Neurosurgery. 2005;57(4 suppl):219-227. specifying the cortical incision over the isthmus cingulum, 17. Klingler J, Gloor P. The connections of the amygdala and of the anterior temporal without compromising the optic radiation that lies lateral to cortex in the human brain. J Comp Neurol. 1960;115(3):333-369. the ventricle. Mahaney and Abdulrauf68 found that the best point 18. Peuskens D, Van Loon J, Van Calenbergh F, van den Bergh R, Goffin J, Plets C. to open the cingulum for this approach is located 5 mm Anatomy of the anterior temporal lobe and the frontotemporal region demonstrated by fiber dissection. Neurosurgery. 2004;55(5):1174-1184. superiorly and laterally to the falcotentorial meeting point. 19. Ferwerda JG. The World of 3-D. 2nd ed. Borger, Netherland: 3-D Book Productions; 2003:210-221. 20. 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Acta Neurochir (Wien). 1992;115(3-4):143-148. 25. Williams PL, Warwick R, eds. Gray’s Anatomy. 36th ed. Philadelphia, PA: The authors have no personal financial or institutional interest in any of the Saunders; 1980. drugs, materials, or devices described in this article. 26. Heimer L. The Human Brain and Spinal Cord: Functional Neuroanatomy and Dissection Guide. 2nd ed. New York, NY: Springer Verlag; 1995. REFERENCES 27. Heimer L. A new anatomical framework for neuropsychiatric disorders and drug abuse. Am J Psychiatry. 2003;160(10):1726-1739. 1. Atlas SW, Howard RS II, Maldjian J, et al. Functional magnetic resonance imaging 28. McGinty JF. Advancing from the ventral to the extended amygdala: of regional brain activity in patients with intracerebral gliomas: findings and implications for neuropsychiatry and drug abuse. Annals of the New York Academy implications for clinical management. Neurosurgery. 1996;38(2):329-338. of Sciences. Vol 877. 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29. Wen HT, Rhoton AL Jr, de Oliveira E, et al. Microsurgical anatomy of the 58. Ikeda K, Shoin K, Mohri M, Kijima T, Someya S, Yamashita J. Surgical temporal lobe, part 1: mesial temporal lobe anatomy and its vascular relationships indications and microsurgical anatomy of the transchoroidal fissure approach for as applied for amygdalohippocampectomy. Neurosurgery. 1999;45:549-592. lesions in and around the ambient cistern. Neurosurgery. 2002;50(5):1114-1120. 30. Rhoton AL Jr. Cranial Anatomy and Surgical Approaches. Schaumburg, IL: 59. Park TS, Bourgeois BF, Silbergeld DL, Dodson WE. Subtemporal trans- Lippincott Williams & Wilkins; 2003. parahippocampal amygdalohippocampectomy for surgical treatment of mesial 31. Peltier J, Travers N, Destrieux C, Velut S. Optic radiations: a microsurgical temporal lobe epilepsy: technical note. J Neurosurg. 1996;85(6):1172-1176. anatomical study. J Neurosurg. 2006;105(2):294-300. 60. Hori T, Tabuchi S, Kurosaki M, et al. 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J Neurol meningiomas with correlative microsurgical anatomy: technical case report. Neurosurg Psychiatry. 1952;15(3):169-183. Neurosurgery. 2005;56(2 suppl):E438. 39. Walsh FB, Hoyt WF. Clinical Neuro-Ophthalmology. 3rd ed. Baltimore, MD: 66. Yas¸argil MG. Microneurosurgery: Microneurosurgery of CNS Tumors.VolIVB. Williams & Wilkins; 1969:43-60. Stuttgart, Germany: Georg Thieme; 1996:313-318. 40. Hervás-Navidad R, Altuzarra-Corral A, Lucena-Martín JA, Castañeda-Guerrero M, 67. Yasargil MG, Türe U, Yasargil DC. Surgical anatomy of supratentorial midline Vela-Yebra R, Sánchez-Alvarez JC. Deficits in the visual field in resective surgery for lesions. Neurosurg Focus. 2005;18(6B):E1. temporal lobe epilepsy [in Spanish]. Rev Neurol. 2002;34(11):1025-1030. 68. Mahaney KB, Abdulrauf SI. Anatomic relationship of the optic radiations to the 41. Hughes B. The . Oxford, UK: Blackwell; 1954. atrium of the lateral ventricle: description of a novel entry point to the trigone. 42. Probst M. Über die zentralen sinnesbahnen und die sinneszentren des Neurosurgery. 2008;63(4 suppl 2):195-203. menschlichen gehirnes. Sber Akad Wiss Wien Math Nat. 1906;K 105:103-112. 43. Marino R, Rasmussen T. Visual field changes after temporal lobectomy in man. Neurology. 1968;18:825-835. COMMENTS 44. Pfeiffer R. Myelogenetisch-anatomische Untersuchungen fiber den zentralen Abschnitt der Sehleitung. Berlin, Germany: Julius Springer; 1925;51-145. he study of white matter tracts of the brain using the technique of fiber 45. Rasmussen AT. The extent of recurrent geniculocalcarine fibers (loop of T dissection as described by Klingler has gained important interest in Archambault and Meyer) as demonstrated by gross brain dissection. Anat Rec. neurosurgical literature over the past decade. Numerous studies have been 1943;85:277-282. presented to illustrate the course of association fibers, commissural fibers, 46. Penfield W. Temporal lobe epilepsy. Br J Surg. 1954;41(168):337-343. and projection fibers and their interaction. This growing interest was 47. Falconer M, Wilson J. Visual field changes following anterior temporal lobectomy: initiated by the emergence of magnetic resonance diffusion tensor imag- their significance in relation to Meyer’s loop of the optic radiation. Brain. 1958;81 ing. This technique allows us to visualize the same white matter tracts (1):1-14. in vivo. Seeing these tracts on magnetic resonance images sparked an in- 48. Sincoff EH, Tan Y, Abdulrauf SI. White matter fiber dissection of the optic radiations of the temporal lobe and implications for surgical approaches to the terest in exploring the brain with the fiber dissection technique in the temporal horn. J Neurosurg. 2004;101(5):739-746. neuroanatomy laboratory. However, as everyone who has experience with 49. Duvernoy HM. The Human Brain: Surface, Three-Dimensional Sectional Anatomy the Klingler dissection technique and with diffusion tensor imaging is and MRI, and Blood Supply. Vienna, Austria: Springer-Verlag; 1999. aware, both techniques are very dependent on the expertise of the in- 50. Türe U, Yas¸argil D, Al-Mefty O, Yas¸argil MG. Topographic anatomy of the vestigator. They very much show what is looked for and therefore should insular region. J Neurosurg. 1999;90(4):720-733. be regarded as illustrative rather than investigative. Nevertheless, both 51. Niemeyer P. The transventricular amygdala-hippocampectomy in temporal lobe techniques help to increase the knowledge of the anatomy of the white epilepsy. In: Baldwin M, Bailey P, eds. The Temporal Lobe Epilepsy. Springfield, IL: matter tracts. This knowledge has become essential for performing surgical Charles C Thomas; 1958;461-482. procedures on the brain. This is especially true for epilepsy surgery and 52. Wieser HG, Yas¸argil MG. Selective amygdalohippocampectomy as a surgical treatment of mesiobasal limbic epilepsy. Surg Neurol. 1982;17(6):445-457. glioma surgery. Because the results of neurosurgical procedures are no 53. Yas¸argil MG, Teddy PJ, Roth P. Selective amygdalo-hippocampectomy: operative longer measured only by evaluating motor function and visual fields but anatomy and surgical technique. Adv Tech Stand Neurosurg. 1985;12:93-123. also by detailed neuropsychological and language testing, it has become 54. Vajkoczy P, Krakow K, Stodieck S, Pohlmann-Eden B, Schmiedek P. Modified clear that every single area of white matter is essential for a normal function approach for the selective treatment of temporal lobe epilepsy: transsylvian- of the human brain. transcisternal mesial en bloc resection. J Neurosurg. 1998;88(5):855-862. The authors present a detailed study of the white matter tracts of the 55. Coppens JR, Mahaney KB, Abdulrauf SI. An anteromedial approach to the temporal and occipital lobe, with emphasis on the optic radiation. Al- temporal horn to avoid injury to the optic radiation fibers and uncinate fasciculus: though the subject has been studied numerous times, the images in this anatomical and technical note. Neurosurg Focus. 2005;18(6B):E3. 56. Choi C, Rubino PA, Fernandez-Miranda JC, Rhoton AL Jr. Meyer’s loop and the work are of superb quality, showing the course of the different tracts in optic radiations in the transsylvian approach to the mediobasal temporal lobe. great detail, in both 2- and 3-dimensional images. Meticulous micro- Neurosurgery. 2006;59(4 suppl 2):ONS228-ONS236. neurosurgical techniques require hours of practice in the laboratory. The 57. Olivier A. Relevance of removal of limbic structures in surgery for temporal lobe same is true for the fiber dissection technique. The authors describe the epilepsy. Can J Neurol Sci. 1991;18(4 suppl):628-635. results of their dissection on 40 hemispheres, whereas other studies

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published were performed on only 20 or 10 hemispheres. Very likely, the optic radiation in vivo,1,2 fiber dissection and 3-dimensional documen- experience gained during these hours in the neuroanatomy laboratory has tation are of high value to surgeons and of significance in terms of led to the expertise that produced such fine results. Moreover, the different information on the relationship between the surgical anatomy and measurements of the course of the optic radiation relative to external physical sensations. landmarks are very helpful in deciding on the right approach to reach the mesial temporal structures and the trigone of the lateral ventricle. Satoru Shimizu Sagamihara, Japan Johannes van Loon Leuven, Belgium

his is an excellent anatomic delineation of the optic radiation. The 3- 1. Taoka T, Sakamoto M, Nakagawa H, et al. Diffusion tensor tractography of the T dimensional images obtained by the authors by laborious and me- Meyer loop in cases of temporal lobe resection for temporal lobe epilepsy: ticulous fiber dissection reveal not only the basic topography but also an correlation between postsurgical visual field defect and anterior limit of Meyer loop unexpected location of the fibers that should be considered at surgery, ie, on tractography. AJNR Am J Neuroradiol. 2008;29(7):1329-1334. 2. Wang YX, Zhu XL, Deng M, et al. The use of diffusion tensor tractography the anterior extended Meyer loop with an anterior edge that was only 20 to measure the distance between the anterior tip of the Meyer loop and the mm from the temporal pole. Although the current status of magnetic temporal pole in a cohort from Southern China. J Neurosurg. 2010;113(6): resonance diffusion tensor tractography makes it possible to depict the 1144-1151.

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