DOI: 10.3171/2008.10.JNS08159

Window anatomy for neurosurgical approaches

Laboratory investigation

Si m e l Ke n d i r , M.D.,1 Ha l i l Ib r a h i m Ac a r , M.D.,1 Ay h a n Co m e r t , M.D.,1 Me v c i Oz d e m i r , M.D., 2 Go k m e n Ka h i l o g u l l a r i , M.D., 2 Al a i t t i n El h a n , D.V.M., Ph.D.,1 a n d Ha s a n Ca g l a r Ug u r , M.D., Ph.D. 2 Departments of 1Anatomy and 2Neurosurgery, Ankara University, Sihhiye, Ankara, Turkey

Object. Knowledge of the cranium projections of the gyral structures is essential to reduce the surgical complica- tions and to perform minimally invasive interventions in daily neurosurgical practice. Thus, in this study the authors aimed to provide detailed information on cranial projections of the eloquent cortical areas. Methods. Ten formalin-fixed adult human were obtained. Using sutures and craniometrical points, the crania were divided into 8 windows: superior frontal, inferior frontal, superior parietal, inferior parietal, sphenoidal, temporal, superior occipital, and inferior occipital. The projections of the precentral gyrus, postcentral gyrus, inferior frontal gyrus, superior temporal gyrus, transverse temporal gyri, Heschl gyrus, genu and splenium of the corpus cal- losum, supramarginal gyrus, angular gyrus, calcarine sulcus, and sylvian fissure to cranial vault were evaluated. Results. Three-fourths of the precentral gyrus and postcentral gyrus were in the superior parietal window. The in- ferior frontal gyrus extended to the inferior parietal window in 80%. The 3 important parts of this gyrus were located below the superior temporal line in all hemispheres. The orbital and triangular parts were in the inferior frontal win- dow, and the opercular part was in the inferior parietal window. The superior temporal gyrus was usually located in the inferior parietal and temporal windows, whereas the supramarginal gyrus and angular gyrus were usually located in the superior and inferior parietal windows. The farthest anterior point of the Heschl gyrus was usually located in the inferior parietal window. The mean positions of arachnoid granulations were measured as 3.9 ± 0.39 cm anterior and 7.3 ± 0.51 cm posterior to the . Conclusions. Given that recognition of the gyral patterns underlying the craniotomies is not always easy, aware- ness of the coordinates and projections of certain gyri according to the craniometric points may considerably contrib- ute to surgical interventions. (DOI: 10.3171/2008.10.JNS08159)

Ke y Wo r d s • gyral anatomy • neurosurgical approach • sulcal anatomy • surgical anatomy • window anatomy

e s p i t e great advances in image-guided technolo- boring the sulci or fissures, which are always persistent gies, studying actual brain structures is still one in the brain, may be very problematic. Therefore, in this of utmost importance. A detailed study of neu- study we especially aimed to highlight the methods to Droanatomy through dissections in cadavers can provide identify the gyri with the guidance of the craniometrical the best orientation in that regard.18,22,24,25,27,28 The modern points and sutures. microneurosurgical approaches mainly require gyri and sulci orientation.3,10,13,20 With the contribution of surgical anatomical studies on the brain surface, several neurosur- Methods gical approaches can be easily performed today.7,8,11,16,17,23 Ten formalin-fixed adult skulls were obtained. Skulls Despite considerable knowledge of intracranial anatomy, with the signs of CNS trauma or disease were excluded. little is known about eloquent brain parts and their The scalp and cranial muscles were removed. The cranial relationships. Cranial-cerebral relationships, firstly de- sutures, lines, and craniometrical points were protected, scribed in the 19th century by Broca, were reevaluated in this study. Misinterpretation of the gyri and sulci pre- and 16,29,30 This article contains some figures that are displayed in color intraoperatively may increase the complication rates. on­line but in black and white in the print edition. Identifying the gyri, especially when they are not neigh-

J. Neurosurg. / April 10, 2009 1 S. Kendir et al. and all the remaining bone tissues were removed with the aid of a high-speed drill (Midas Rex Legend Gold Touch) (Fig. 1). The arachnoid granulations and branches of mid- dle meningeal artery on the dura mater were observed (Fig. 2). Then, the dura mater was removed and the cortical structures were inspected. The procedure disclosed 8 win- dows in each hemisphere: superior frontal, inferior frontal, superior parietal, inferior parietal, sphenoidal, temporal, superior occipital, and inferior occipital windows (Fig. 1). The projections of the precentral gyrus, postcentral gyrus, inferior frontal gyrus, superior temporal gyrus, transverse temporal gyri, Heschl gyrus, genu and splenium of the cor- pus callosum, supramarginal gyrus, angular gyrus, calcar- ine sulcus, and sylvian fissure on the windows were evalu- ated. Because these important cortical areas were located in 5 of the 8 windows when craniotomies were performed, these 5 windows (inferior frontal, superior parietal, inferior parietal, and temporal and superior occipital) were taken into consideration during evaluation. To perform a detailed Fig. 2. Photograph, superior view, showing the branches of the middle investigation of the parts of the inferior frontal gyrus, the meningeal artery on the dura mater, locations of the arachnoid granula- sulci that separated the parts were used. The locations of tions, and their distances. SS = sagittal suture. the arachnoid granulations through the sagittal sinus were observed. The morphometric measurements were done shrinkage; however, the distances of the gyrus located far from the bone to the midgyral point. The measurements from the middle of the cerebrum, such as the orbital part were obtained using a measuring tape (precision 0.1 mm), of inferior frontal gyrus, may be affected more. and a standard goniometer (precision 1°) was used for angular measurements. An analysis of the measurements Results (mean ± SD) was also performed. Shrinkage of the cerebral hemispheres may occur at Precentral Gyrus the time of fixation. Given that the reference points and The precentral gyrus was located 4.5 cm (right 4.34 the direction of measurements varied according to the ± 1.06 cm, left 4.66 ± 0.91 cm) behind the bregma on gyrus examined, a constant linear correction factor was the midline (Fig. 3) and coursed laterally and frontally, not used in this study. Thus, the sagittal distances of a creating a 59° (right 58.8 ± 5.49°, left 59.2 ± 4.37°) angle gyrus located close to the middle of the cerebrum, such as with the sagittal suture. Three-fourths of the precentral precentral gyrus, will not be significantly affected by the gyrus was in the superior parietal window. At the lower margin of the inferior parietal window, the gyrus reached

Fig. 1. Photograph showing the exposure of the cranium, cranial sutures (coronal [CS], lambdoid [LS], and squamous [SqS] sutures, and superior temporal line [STL]) and craniometric points (bregma [B], stephanion [S], [P], [L], and [A]) in the cadaver Fig. 3. Photograph showing the relationships and distances of the skulls. Craniotomies disclose the following 8 windows on each side: precentral gyrus in the superior and inferior parietal windows with the superior frontal (1), inferior frontal (2), sphenoidal (3), superior parietal craniometric points (bregma, stephanion, and pterion) and cranial su- (4), inferior parietal (5), temporal (6), superior occipital (7), and inferior tures (coronal, sagittal, and squamous sutures, and superior temporal occipital (8). line).

2 J. Neurosurg. / April 10, 2009 Window anatomy for neurosurgical approaches

Fig. 5. Photograph showing the relationships and distances of the Fig. 4. Photograph showing the relationships and distances of the angular gyrus (AG), supramarginal gyrus (SMG), and parts of the in- postcentral gyrus in the superior and inferior parietal windows with the ferior frontal gyrus (orbital [Or], triangular [Tr], and opercular [Op]) with craniometric points (bregma, stephanion, pterion, and lambda) and the craniometric points (bregma, stephanion, pterion, lambda, and as- cranial sutures (coronal, sagittal, and squamous sutures, and superior terion) and cranial sutures (coronal, sagittal, squamous, and lambdoid temporal line). sutures, and the superior temporal line). the sylvian fissure. The precentral gyrus extended to the ascending rami) were used to separate the inferior fron- temporal window in some hemispheres (30%). On the lat- tal gyrus into 3 parts: orbital, triangular, and opercular. eral surface, the gyrus was only 2.5 cm (right 2.46 ± 0.63 The locations of these 3 important parts were below the cm, left 2.54 ± 0.54 cm) behind the stephanion (Fig. 3). superior temporal line in all the hemispheres. The orbital In most cases (80%), the precentral gyrus was a strip that and triangular parts were in the inferior frontal window, had no connection with other gyri. and the opercular part was in the inferior parietal window (Fig. 5). The triangular part could be seen in the inferior Postcentral Gyrus parietal window (left 60%, right 50%) (Fig. 5), and the The postcentral gyrus was located 6.5 cm (right 6.50 opercular part could be seen in inferior frontal window ± 0.68 cm, left 6.50 ± 0.65 cm) behind the bregma on the (left 30%, right 40%). The triangular part was located 1.9 midline (Fig. 4) and coursed laterally and frontally con- cm (right 2.34 ± 1.42 cm, left 1.38 ± 0.63 cm) anterior to stituting a 62° (right 61.9° ± 4.33, left 62.1 ± 4.38°) angle the coronal suture. The triangular part was located 1.4 with the sagittal suture. Three-fourths of the postcentral cm (right 0.97 ± 0.54 cm, left 1.85 ± 0.79 cm) below the gyrus was in the superior parietal window. At the lower superior temporal line. margin of the inferior parietal window, the gyrus reached to the sylvian fissure. The postcentral gyrus extended to Superior Temporal Gyrus, Transverse Temporal Gyri, and the temporal window in some hemispheres (10%). On the Heschl Gyrus lateral surface, the gyrus was located 4.1 cm (right 4.07 ± In all hemispheres, the superior temporal gyrus was 0.52 cm, left 4.13 ± 0.45 cm) behind the stephanion (Fig. located in the inferior parietal and temporal windows, ex- 4). In most of the cases (90%), the postcentral gyrus was a cept in 1 hemisphere (5%), in which it was seen in the strip that had no connection with other gyri. superior parietal window; the crossing point of this gyrus Inferior Frontal Gyrus with the superior temporal line was located 7.9 cm behind the stephanion. The end of the inferior frontal gyrus was noted near The transverse temporal gyrus constitutes the poste- the stephanion, 1.9 cm (right 1.97 ± 1.04 cm, left 0.89 ± rior part of the upper surface of the temporal lobe, which 0.54 cm) posterior to the coronal suture (Fig. 5). Although is known as the temporal plane. The farthest anterior the inferior frontal gyrus extended to the inferior parietal point of the temporal plane, which was also the anterior window in 80% of the cases, it extended to the superior boundary of the Heschl gyrus, was usually located in the parietal window in 20%. In the cases in which the inferior inferior parietal window. This point was placed on the frontal gyrus extended to the superior parietal window, same vertical line with the beginning point of the ascend- the end of the gyrus was located 0.7 cm (right 0.70 ± 0.14 ing ramus of the sylvian fissure and in 1 specimen, the cm, left 0.70 ± 0.18 cm) above the superior temporal line. point was located in the temporal window. The posteri- In cases in which the inferior frontal gyrus extended to or-most boundary of the transverse temporal gyrus was the inferior parietal window, the end of this gyrus was 1.8 in the area where the posterior ramus of the sylvian fis- cm (right 2.00 ± 0.75, left 1.70 ± 0.58 cm) below this line sure curved upward. This point was located in the third (Fig. 5). The sylvian fissure and its branches (anterior and quarter of the inferior parietal window in all cases. The

J. Neurosurg. / April 10, 2009 3 S. Kendir et al. anterior-most point of the temporal plane was found 2.8 Corpus Callosum cm (right 2.92 ± 0.80 cm, left 2.61 ± 0.80 cm) inferior to The distance between the and genu of the cor- the superior temporal line. This point was located 0.8 cm pus callosum was measured as 12.6 ± 0.44 cm, and the (right 0.62 ± 0.15 cm, left 0.93 ± 0.39 cm) posterior to the distance between the nasion and splenium of corpus cal- coronal suture. losum was 19.8 ± 0.82 cm. Supramarginal Gyrus The point at which the sylvian fissure ended, which Discussion terminates in the middle of the supramarginal gyrus, was Proper craniotomy of a brain lesion and correct in- noted in order to evaluate the location of the gyrus. In terpretation of the gyral structures under the cranioto- all the hemispheres, this point was seen in the superior my site is one of the most important steps in successful and inferior parietal windows. It was located 6.0 cm (right surgery.1,2,20,25 There are very few persistent sulci in the 6.03 ± 1.49 cm, left 6.04 ± 0.70 cm) in front of the lamb- brain that are always present in every individual. There- doid suture. The distance between this point and the sag- fore, identification of gyral structures may not be easy. To ittal suture was 6.7 cm (right 6.83 ± 1.28 cm, left 6.59 ± identify these structures, the use of bone structures of the 1.32 cm) on the lateral surface of the hemisphere (Fig. 5). cranium may prove to be beneficial. To this end, in our The crossing point of the sylvian fissure with the superior study a window anatomy model was developed. temporal line was located 6.4 cm (right 6.40 ± 0.83 cm, The linear correction factors of 0.88–0.94 can be de- left 6.39 ± 0.88 cm) behind the stephanion in 12 hemi- termined at the usual fixation in ~ 4% formalin.14 How- crania (right 4, left 8) (Fig. 5). In 80% of the cases, the ever, the measurements refer to a relatively small number supramarginal gyrus was seen under the parietal tuber. of cases. Given that the measurements were obtained af- ter 10% formalin fixation, calculations of absolute linear Angular Gyrus measurements had to include ~ 0.9 as a shrinkage correc- The end of the superior temporal sulcus, which ter- tion factor in the present study. Since the reference points minates in the middle of the angular gyrus, was consid- and the direction of measurements varied according to ered to evaluate the location of the gyrus. In all the hemi- the gyrus examined, a constant linear correction factor spheres, this point was seen in the superior and inferior was not used in this study. parietal windows. It was located 4.3 cm (right 4.39 ± 1.21 A reliable identification of functional cortical ar- cm, left 4.16 ± 1.00 cm) in front of the lambdoid suture eas can be achieved through preoperative cortical map- 10,21,26,29 (Fig. 5). The distance between this point and the sagittal ping. In addition, the combination of the data suture was 5.0 cm (right 5.01 ± 1.39 cm, left 5.00 ± 1.42 obtained from neuronavigation systems and functional cm) on the lateral surface of the hemisphere (Fig. 5). The MR imaging evaluations may provide information on 12,15 crossing point of superior temporal sulcus with superior the functional cortical areas. The integration of sul- temporal line was 8.4 cm (right 8.33 ± 0.55 cm, left 8.45 ± cal and functional information of the brain and the im- portance of imaging were described by Jannin et al.6 In 0.54 cm) behind the stephanion. In 20% of the cases, the 4 angular gyrus was located under the parietal tuber. another study, Gong et al. described some cortical area findings obtained through diffusion weighted MR imag- Calcarine Sulcus ing techniques. The MR imaging techniques can also be used for superficial brain lesions in the precentral gyrus, The end of calcarine sulcus on superolateral surface as described by Hattingen et al.5 This study reformatted was observed 4.4 cm (right 4.50 ± 1.02 cm, left 4.30 ± 1.13 images for fast and easy determination of the locations of cm) inferior and 1.7 cm (right 2.00 ± 0.80 cm, left 1.41 ± the precentral gyrus and perirolandic lesions. A similar 0.64 cm) lateral to the lambda. The turning point of cal- study was reported by Krishnan et al.9 In that study, the carine sulcus from the superolateral surface to the medial authors described the functional MR imaging–integrated surface was different on the right and left hemispheres. neuronavigation for correlation between the cranial lesion The location of this point was 4.0 cm (right 4.00 ± 0.82 and motor cortex, which was one of the objectives of our cm, left 3.90 ± 0.76 cm) inferior and 0.7 cm (right 1.01 ± study. Although we have used MR imaging assistance in 0.23 cm, left 0.40 ± 0.26 cm) lateral to the lambda. surgical practice, the study itself focused on the detec- Arachnoid Granulations tion of the important cortical areas by using craniometric points in the . This detailed anatomical information Arachnoid granulations were accumulated around may prove useful in finding and interpreting the areas un- (especially behind) the bregma (Fig. 2). The superficial der the bone. veins of the hemispheres drained into these granulations. The positive contribution of advanced technology The area comprising these granulations was supplied by to surgical outcome is undeniable. However, it is also an the branches of the middle meningeal artery (Fig. 2). In undeniable fact that anatomical knowledge and 3D orien- all the skulls, the positions of arachnoid granulations tation are indispensable for successful surgical outcome. were measured as 3.9 ± 0.39 cm anterior and 7.3 ± 0.51 Another indication for the importance of anatomical cm posterior to the bregma (Fig. 2). These structures were knowledge is the fact that advanced technology is not al- located 2.6 cm (right 2.40 ± 0.43 cm, left 2.77 ± 0.33 cm) ways available and applicable.15,16 laterally to the sagittal suture (Fig. 2). One end of the precentral and postcentral gyri is in

4 J. Neurosurg. / April 10, 2009 Window anatomy for neurosurgical approaches the interhemispheric fissure, and the other end is in the da, and because of its proximity to the confluence of si- sylvian fissure. These gyri project forward with an angle nuses, it can easily be recognized during surgery. Howev- of 60°. Thus, their reflections on the midline are signifi- er, it should be kept in mind that the confluence of sinuses cantly different from those of the sylvian fissure. Conse- in particular may deviate 2 cm from the midline to the quently, a craniotomy closer to the midline will have a right, and thus, the calcarine sulcus may deviate from the different motor and sensorial cortex orientation from that midline on the right. of a craniotomy closer to the sylvian fissure. The closer the precentral gyrus is to the sylvian fissure, the closer it is to the coronal suture, with the distance reducing to as Conclusions much as 2.8 cm at the stephanion. Given that recognition of the gyral patterns underly- The sylvian fissure is a very important corridor for ing the craniotomies is not always easy, awareness of the neurosurgical interventions.13,22,19,20 The anterior and as- coordinates and projections of certain gyri according to cending rami are of great importance in defining the in- the craniometric points may considerably contribute to ferior frontal gyrus, and the posterior ramus is important surgical intervention. in defining the supramarginal gyrus. If the rami of the sylvian fissures are not observed in the craniotomy area Disclaimer preoperatively, the definition of these gyri may be highly The authors report no conflict of interest concerning the mate- challenging. In that case, the presence of inferior frontal, rials or methods used in this study or the findings specified in this precentral, and postcentral gyri in the area on the supe- paper. rior temporal line (in other words, in the inferior parietal window) should be kept in mind. No sulcal structures ex- Acknowledgments ist that will aid in defining the angular and supramarginal gyri. Particularly when the posterior ramus of the sylvian The authors thank Prof. Dr. S. Tuna Karahan and Prof. Dr. Ibra­ fissure is not observed in the craniotomy area, it is impor- him Tekdemir (Department of Anatomy, Ankara University Faculty tant to know that the area behind the external ear canal, of Medicine) for their invaluable contributions and Mrs. Safak Ugur where the inferior parietal and superior parietal windows for her editorial assistance. merge, is where the supramarginal and angular gyri are located. 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