Surg Radiol Anat DOI 10.1007/s00276-014-1294-6

Original Article

Sulcal and gyral anatomy of the basal occipital–temporal lobe Anthony Minh Tien Chau · Fiona Stewart · Cristian Gragnaniello 

Received: 19 February 2014 / Accepted: 31 March 2014 © Springer-Verlag France 2014

Abstract  Purpose The sulcal and gyral anatomy of the basal occipital–temporal lobe is highly variable and detailed descriptions of this region are limited and often inconsistent. The aim of this study was to describe the salient features of the sulcal and gyral anatomy of the basal occipital–temporal lobe. Methods  We studied the sulcal and gyral patterns of 30 formalin-fixed cerebral hemispheres. Results The major landmarks are the collateral sulcus (separated into the rhinal, proper, and caudal segments) and occipitotemporal sulcus (often interrupted), which were always present in this study. The bifurcation of the caudal collateral sulcus is a useful landmark. In relation to these sulci, we have described the surface anatomy and nominated landmarks of the medial (parahippocampal and lingual) and lateral (fusiform) occipitotemporal gyri. Conclusions  Understanding of the sulcal and gyral patterns of the basal occipital–temporal lobe may provide valuable information in its radiological and intraoperative interpretation.

Keywords Neuroanatomy · Temporal lobe · Occipital lobe

Introduction The sulcal and gyral anatomy of the basal occipital–temporal lobe is highly variable and detailed descriptions of this region are often inconsistent. Three reliable landmarks exist which delineate the regions and identify the structures of the basal occipital–temporal lobe—the rhinal, collateral, and occipitotemporal sulci. Terminology for these varies between the texts [4]. Few gross anatomical studies dedicated to describing basal occipital–temporal lobe sulcal and gyral anatomy exist in the literature. Definitions of the rostrocaudal borders of the medial and lateral occipitotemporal gyri, and descriptions of the collateral sulcus bifurcation in the wet specimen are difficult to obtain. In this paper, we seek to address these deficiencies and identify anatomical landmarks through gross examination of post-mortem light formalin-fixed brains.

Materials and methods

A. M. T. Chau (*) · C. Gragnaniello  Macquarie Neurosurgery, Australian School of Advanced Medicine, Macquarie University Hospital, Macquarie University, Suite 201, Level 2, 2 Technology Place, Sydney, NSW 2109, Australia e-mail: [email protected] A. M. T. Chau · F. Stewart · C. Gragnaniello  School of Medicine, University of New England, Armidale, NSW, Australia

The sulcal and gyral patterns of 30 formalin-fixed cerebral hemispheres were studied. The sample consisted of 15 adult brains (nine males, six females), mean age 75 years (range 49–96 years). No significant cerebral disease was noted on their cause of death or on gross anatomical inspection. Digital photographs of the sulcal patterns were taken and data entered into a spreadsheet. The collateral sulcus terminology framework proposed by Huntgeburth and Petrides [4] was adopted for this study. Institutional ethics approval was obtained prior to commencement of this study.

13



Results

Surg Radiol Anat

projection continued posteriorly as the lingual gyrus, which terminated at the occipital cortex.

Gyral anatomy Lateral occipitotemporal gyrus (fusiform gyrus) Medial occipitotemporal gyrus The medial occipitotemporal gyrus consists of the parahippocampal and lingual gyri, approximately defined via a coronal line taken at the level of the cingulate isthmus and splenium of the corpus callosum (Figs. 1, 2a–a′). The anterior parahippocampal gyrus includes the entorhinal region and angular gyrus. In this region, an intrarhinal “nick” indicates the impression of the cerebellar tentorium upon the medial basal temporal surface forming the lateral border of the ambient gyrus. This nick was present in 28 (93 %) hemispheres. A short rostrocaudal entorhinal sulcus within the entorhinal region was identified in 3 (10 %) hemispheres. The parahippocampal gyrus projected anteriorly to the temporal pole, anteromedially to the uncus, and posteromedially to blend with the cingulate isthmus. This gyral

The lateral occipitotemporal, or fusiform gyrus, is named due to its spindle-like shape. Using the afore-mentioned coronal line, taken at the level of the cingulate isthmus and splenium of the corpus callosum (Fig. 2a–a′), the gyrus was divided into anterior and posterior sections. In all specimens, the medial and lateral borders were well defined by the collateral and occipitotemporal sulci, respectively. The fusiform gyrus’ anterior and posterior borders were less well defined. Anteriorly, the gyrus extended into the temporal pole to its “limit”, the ventral-most part of the occipitotemporal sulcus. Posteriorly, the fusiform gyrus ended, together with the lingual and inferior temporal gyri, at the occipital cortex. The fusiform’s mean length was 75 mm (SD 7 mm). In 7 hemispheres (23 %), the fusiform gyrus had no associated short sulci. In 8 (27 %) hemispheres, one short sulcus was identified (Fig. 3); in 6 (20 %) hemispheres, there were 2 short sulci; in 7 (23 %) hemispheres, there were three short sulci, and in 2 (6 %) hemispheres, there were four short sulci. Sulcal anatomy Collateral sulcus The collateral sulcus was present in all specimens. It ran rostrocaudally from the anterior-medial temporal basal region to the occipital lobe, separating the parahippocampal and lingual gyri, medially, from the fusiform gyrus, laterally. Huntgeburth divided the collateral sulcus into three distinct regions: an anterior segment, commonly named the rhinal sulcus; a middle segment, the collateral sulcus proper, and a posterior segment, the caudal occipital sulcal segment.

Fig. 1  Inferomedial view of the basal occipital–temporal lobe. A coronal line (a–a′) at the level of the cingulate isthmus divides the parahippocampal and lingual gyrus, whilst dividing the fusiform gyrus into anterior and posterior segments. The line (b–b′) is the temporo-occipital line which delineates the basal temporal and occipital lobes, indicating the posterior limit of the bifurcation of the collateral sulcus, with its medial and lateral rami. The parahippocampal gyrus projects anteromedially to the uncus and posteromedially to blend in with the cingulate isthmus, and continues as the lingual gyrus at the level of the splenium/cingulate isthmus. Legend—AG ambient gyrus, Calc sul calcarine sulcus, CCS caudal collateral sulcus, Cing isth cingulate isthmus, CSP collateral sulcus proper, ER entorhinal cortex, FG fusiform gyrus, ITG inferior temporal gyrus, LG lingual gyrus, OCx occipital cortex, OTS occipital temporal sulcus, PHG parahippocampal gyrus, PHR parahippocampal ramus, POF parietooccipital fissure, PON preoccipital notch, RS rhinal sulcus, TOL temporooccipital line connecting the tip of the parietooccipital fissure to the preoccipital notch, TP temporal pole, Un uncus

13

Rhinal sulcus  The rhinal sulcus occupies the ventromedial temporal lobe. It courses between the entorhinal cortex of the anterior parahippocampal gyrus and the anterior fusiform gyrus. It was present in all specimens. Its length was on average 25 mm (SD 4 mm) and its mean maximal depth 13 mm (SD 3 mm). Posteriorly, the rhinal sulcus ended at the level of the anterior border of the midbrain. This sulcus demonstrated variation with respect to side branches which were lateral, or medial, or both lateral and medial. In 12 specimens (40 %), the rhinal sulcus gave rise to short side branches; in ten (33 %) specimens, there were short lateral branches (Fig.  4). In each of the other specimens examined, one (3 %) displayed lateral and medial branches; another

Surg Radiol Anat

Fig. 2  Illustration demonstrating the features of the basal occipital– temporal lobe. a inferior view, b medial view. A coronal line (red dotted line) taken at the level of the cingulate isthmus and splenium of the corpus callosum, defines the two halves of the medial and lateral occipitotemporal gyri. The collateral sulcus proper is thereby divided into the rhinal sulcus, the collateral sulcus proper, and the caudal (occipital) collateral sulcus. Ant FG anterior fusiform gyrus, Cisth

cingulate isthmus, CS collateral sulcus, IRN intrarhinal nick, ITG inferior temporal gyrus, LG lingual gyrus, MB midbrain, OTS occipitotemporal sulcus, PHG parahippocampal gyrus, PHR parahippocampal ramus, Post FG posterior fusiform gyrus, RS rhinal sulcus, TOL temporo-occipital line (blue dotted line), TP temporal pole, Un uncus (color figure online)

specimen (3 %) displayed ventromedial, ventrolateral and posterolateral side branches. In another hemisphere (3 %), the rhinal sulcus was joined laterally by the anterior end of the occipitotemporal sulcus (Fig. 3).

presence of a bridging gyrus (Fig. 2). In 5 (17 %) hemispheres, the collateral sulcus proper commenced posterior to the rhinal sulcus after a short interruption (non-overlapping). In 15 (50 %) hemispheres, a parahippocampal ramus was present (Fig. 5). It commenced medially near the posterior midbrain and ran posterolaterally to its connection with the collateral sulcus proper. It accommodated a temporal artery, usually the common temporal artery, which arose from the third segment of the posterior cerebral artery.

Collateral sulcus proper  The collateral sulcus proper separated the posterior parahippocampal gyrus from the anterior fusiform gyrus and first part of the posterior fusiform gyrus (Figs. 2, 6). It extended approximately from the level of the anterior, or lateral border of the midbrain to the temporo-occipital line which delineated the temporal and occipital lobes. The temporo-occipital line was defined as a line connecting the tip of the parieto-occipital fissure, medially, to the preoccipital notch (temporo-occipital incisure) laterally. In 15 (50 %) hemispheres, the collateral sulcus proper was continuous, anteriorly, with the rhinal sulcus (Fig. 3). In 10 (33 %) hemispheres, it commenced lateral to, overlapping, the posterior end of the rhinal sulcus due to the

Caudal (occipital) collateral sulcus  The caudal collateral sulcus commenced at the bifurcation of the collateral sulcus or from the temporo-occipital line, and extended to its termination near, or at the occipital cortex. It separated the lingual gyrus, medially, from the posterior fusiform gyrus, laterally. In 26 (87 %) hemispheres, the caudal collateral sulcus bifurcated into medial and lateral rami. This bifurcation occurred at the level of the cingulate isthmus in the

13



Surg Radiol Anat

Fig. 4  Basal surface of the right anterior temporal lobe, demonstrating a short lateral branch arising from the rhinal sulcus (RS)

Fig. 3  Basal surface of the right occipital–temporal lobe. In this hemisphere, the anterior occipitotemporal sulcus (OTS) anastomoses with the rhinal sulcus (RS), which is continuous with the collateral sulcus (CS) proper. The medial ramus of the caudal collateral sulcus is the intralingual sulcus. A deep transverse sulcus crosses the fusiform gyrus (FG), producing the unusual trifurcated caudal collateral sulcal appearance

temporal lobe (16 hemispheres, 53 %) or, just posterior to it at, or before, the temporo-occipital line (47 %). The coordinates of the bifurcation point were relatively consistent in the formalin-fixed brain with a mode 20 mm from the midline (mean 21 mm, SD 4 mm, range 15–34 mm), and mode 50 mm from the occipital pole (mean 49 mm, SD 5 mm, range 34–57 mm) (Fig. 6). Intralingual sulcus In 29 (97 %) hemispheres, the lingual gyrus contained at least one intralingual sulcus. In 14 (47 %) hemispheres, the medial ramus of the caudal collateral sulcus formed the

13

Fig. 5  Basal surface of the right occipital–temporal lobe. The common temporal artery is raised upon the probe revealing the parahippocampal ramus (PHR). This ramus extends posterolaterally beginning from the ambient cistern, and anastomosing with the collateral sulcus (CS) proper. The uncus, with an indentation from the tentorium cerebelli, is visible (the intrarhinal nick). In this specimen, the caudal collateral sulcus does not bifurcate, and there is a free longitudinal intralingual sulcus present

intralingual sulcus (Fig. 7). In 10 (33 %) hemispheres, a sulcus ran rostrocaudally, but was not associated with the collateral sulcus (Fig. 5). In 3 (10 %) hemispheres, there

Surg Radiol Anat

Fig. 7  Section of the left basal temporal lobe at the level of the cingulate isthmus, showing the lateral and medial (intralingual) collateral sulci as they bifurcate from the collateral sulcus proper. CS collateral sulcus, ITG inferior temporal gyrus, LG lingual gyrus, MB midbrain, OTS occipitotemporal sulcus, PHG parahippocampal gyrus, PHR parahippocampal ramus, FG fusiform gyrus, RS rhinal sulcus

Fig. 6  Right basal occipital–temporal lobe with emphasis on the caudal collateral sulcus (CS) bifurcation. In this specimen, the bifurcation of the collateral sulcus proper to the medial and lateral caudal collateral sulci occurs anterior to the temporo-occipital line (b–b′), which demarcates the temporal and occipital lobes. When measured, it occurred at approximately 20 mm from the midline and 50 mm from the occipital pole. MB midbrain, RS rhinal sulcus, OTS occipitotemporal sulcus

was a free transverse sulcus. In one (3 %) hemisphere, both a rostrocaudal and a free transverse sulcus were present. Occipitotemporal sulcus The occipitotemporal sulcus separated the fusiform gyrus, medially, from the inferior temporal gyrus, laterally. It was always present. This sulcus ran in a curvilinear manner from the temporal to occipital poles. In the specimens

examined, its mean length was 81 mm (SD 16 mm, range 57–110 mm) and its mean maximal depth was 15 mm (SD 3 mm). This sulcus ran uninterrupted in 9 (30 %) hemispheres, in 13 (43 %) hemispheres it displayed one interruption, in 4 hemispheres (13 %) there were two interruptions, and in 4 (13 %) hemispheres there were three interruptions. As previously described, the occipitotemporal sulcus connected anteriorly with the rhinal sulcus in one hemisphere (3 %) (Fig. 3). In 12 (40 %) hemispheres, the posterior end of the occipitotemporal sulcus joined the lateral ramus of the caudal collateral sulcus.

Discussion The morphological appearance of the basal occipital– temporal lobe, based upon the examination of 30 cerebral hemispheres, has been described. The major landmarks are the collateral sulcus (separated into the rhinal, proper, and caudal segments) and occipitotemporal sulcus (often interrupted), which were always present in this study. In relation to these sulci, we have described the surface anatomy of

13



the medial (parahippocampal and lingual) and lateral (fusiform) occipitotemporal gyri. We suggest that the basal occipital–temporal lobe be segmented via a coronal line at the level of the cingulate isthmus. This line separates the parahippocampal gyrus from the lingual gyrus, and splits the fusiform gyrus into anterior and posterior segments. At that level (53 %) or just posterior to it (at, or before the temporo-occipital line), the caudal collateral sulcus generally bifurcates into its medial and lateral rami. Our division of the basal occipital–temporal lobe is not at great variance from that proposed by earlier authors who studied the medial basal temporal lobe [1, 2]. These authors have trisected the medial temporal region at the levels of the inferior choroidal point and quadrigeminal plate. We have nominated the cingulate isthmus as a bisecting point because it provides a simplified anatomical framework focused primarily upon major sulcal and gyral landmarks of the entire occipital temporal basal region, as above mentioned. Our cadaver analysis of morphology of the sulcal patterns of the basal occipital–temporal lobe identifies a number of important anatomical patterns in the collateral sulcus. In the anterior region, we found a high rate of continuity between the rhinal sulcus and the collateral sulcus proper (50 %). This exceeds the frequency reported by Ono et al. [7] in their series of 25 brains (28 %), and Novak et al. [6] in their series of 50 MRI scans of patients with temporal lobe epilepsy (33 %). Our observations were similar to those of Hanke who found an incidence of 41 % [3]. In an MRI series, Kim et al. [5] found a statistically higher incidence of the connected sulcal pattern in temporal lobe epilepsy (75 %) in comparison with control patients (44 %). The clinical significance of this “simplified” sulcal pattern is unclear, but it has been suggested to predispose to epilepsy [5]. In the middle collateral proper sulcus region, the parahippocampal ramus was a surface landmark in 50 % of hemispheres. When present, it typically accommodated the common temporal artery, the major feeding vessel to the basal temporal region, which usually arose from the third segment of the posterior cerebral artery. In the caudal collateral sulcus region, we confirmed and further described the reliable occurrence of the bifurcation of the posterior collateral sulcus into posteromedial and posterolateral rami (87 %). As noted by Huntgeburth and Petrides [4], the bifurcation point was frequently at the level of the cingulate isthmus (91 % in their study, 53 % in this study). Some authors have speculated that during development, the anterior branch of an intralingual sulcus may shift anterolaterally and join the collateral sulcus

13

Surg Radiol Anat

proper, forming a bifurcation [4, 7]. In our examination, 47 % of the medial collateral sulci were intralingual sulci. Our descriptions of the afore-mentioned surface landmarks add to the limited current data, and it may correlate with sulcal and gyral patterns seen on MRI, and in the intraoperative evaluation of neurosurgical patients. For example, in procedures such as selective amygdalohippocampectomy, via the transsylvian transventricular approach for intractable epilepsy, an understanding of the variant connections between the rhinal and collateral proper sulci may be crucial [9]. The collateral sulcus proper forms an indentation into the temporal horn, the collateral eminence, which is used to identify the fusiform gyrus and the lateral limits for resection. In surgical cases where the collateral sulcus proper and the rhinal sulcus overlap, producing bridging gyri (33 % in this study), or where an anteriorly connecting occipitotemporal gyrus with its associated ventricular indentation occurs (3 %), the lateral limits of the parahippocampal gyrus may be difficult to identify. The consequences include incomplete parahippocampal resection, or inadvertent removal of the medial fusiform gyrus [6, 9]. The functional sequelae of the latter may include prosopagnosia or dyslexia. Yet another example may be in the context of approaching the mediobasal temporal region via the paramedian supracerebellar transtentorial approach, where, for that surgical approach, the caudal collateral sulcus provides the major anatomical landmark [8]. We found the coordinates of the caudal collateral bifurcation to be relatively consistent (in the formalin-fixed brain) at 20 mm from the midline, and 50 mm from the occipital pole—occurring at approximately the level of the cingulate isthmus. An appreciation of this morphology may be helpful in localizing and identifying the transition point between the parahippocampal and lingual gyri, and in identifying the medial border of the fusiform gyrus, when accessing that region via a narrow surgical corridor.

Conclusion Current literature is scarce in studies of the anatomy of the basal occipital–temporal lobe in the wet specimen. Based on the gross anatomical inspection of light formaldehyde-fixed cadaver brains, we have described and nominated boundaries and landmarks for the medial and lateral occipitotemporal gyri. In addition, we have examined and described the collateral sulcus, which we have found to be a dependable, and predictably variable, anatomical landmark. Acknowledgement of its variations may provide valuable information in intraoperative interpretation of neurosurgical landmarks.

Surg Radiol Anat Acknowledgments The authors are indebted to the altruism and generosity of the individuals who donated their bodies to science. Conflict of interest  All authors declare that no actual or potential conflict of interest exists.

References 1. Campero A, Troccoli G, Martins C, Fernandez-Miranda JC, Yasuda A, Rhoton AL Jr (2006) Microsurgical approaches to the medial temporal region: an anatomical study. Neurosurgery 59:ONS-279–ONS-307 discussion ONS-8 2. de Oliveira E, Tedeschi H, Siqueira MG, Ono M, Rhoton AL Jr, Peace D (1994) Anatomic principles of cerebrovascular surgery for arteriovenous malformations. Clin Neurosurg 41:364–380 3. Hanke J (1997) Sulcal pattern of the anterior parahippocampal gyrus in the human adult. Ann Anat 179:335–339 4. Huntgeburth SC, Petrides M (2012) Morphological patterns of the collateral sulcus in the human brain. Eur J Neurosci 35:1295–1311

5. Kim H, Bernasconi N, Bernhardt B, Colliot O, Bernasconi A (2008) Basal temporal sulcal morphology in healthy controls and patients with temporal lobe epilepsy. Neurology 70:2159–2165 6. Novak K, Czech T, Prayer D, Dietrich W, Serles W, Lehr S, Baumgartner C (2002) Individual variations in the sulcal anatomy of the basal temporal lobe and its relevance for epilepsy surgery: an anatomical study performed using magnetic resonance imaging. J Neurosurg 96:464–473 7. Ono M, Kubik S, Abernathey CD (1990) Atlas of the cerebral sulci. Thieme Medical Publishers, New York 8. Ture U, Harput MV, Kaya AH, Baimedi P, Firat Z, Ture H, Bingol CA (2012) The paramedian supracerebellar-transtentorial approach to the entire length of the mediobasal temporal region: an anatomical and clinical study. Laboratory investigation. J Neurosurg 116:773–791 9. Yasargil MG, Krayenbuhl N, Roth P, Hsu SP, Yasargil DC (2010) The selective amygdalohippocampectomy for intractable temporal limbic seizures. J Neurosurg 112:168–185

13

Sulcal and gyral anatomy of the basal occipital-temporal lobe.

The sulcal and gyral anatomy of the basal occipital-temporal lobe is highly variable and detailed descriptions of this region are limited and often in...
1MB Sizes 4 Downloads 3 Views