Temporal Artery and Temporal Region Supplied by the Middle Cerebral Artery: An Anatomical Study

Abstract: This study was conducted to describe in detail the branching patterns of cortical branches from the middle cerebral artery supplying the feeding of the temporal region, to define the arterial structure of temporal artery (TA) and to determine the effect of this arterial supply to the temporal region. The arteries of brains (n.22; 44 hemispheres) were prepared for dissection after filling them with colored latex. TA was defined, and its classification was described, specifying its relationship with other cortical branches. A new classification was defined related to TA terminology. TA was found in 95% of cadavers, and it originated as an early branch in 75% and from the inferior trunk in 24% of cadavers. TA was classified as Type 0: No TA, Type I: single branch providing two cortical branches, Type II: single branch providing three or more cortical branches and Type III: double TA. Type I-TA (45%) was the most common, and Type II-TA arterial diameter was significantly larger than that of other types. All cadavers showed the cortical branches of temporal region from middle cerebral artery, anterior TA , middle TA, posterior TA and temporooccipital artery, except temporopolar artery (81%). Temporopolar artery, anterior TA, and middle TA primarily originated from TA, an early branch, but posterior TA and temporooccipital artery primarily originated from the inferior trunk. Detailed knowledge about cortical branches together with TA and also this region’s blood supply would enable increased prediction of complications, especially in cases with these region-related pathologies, and would make interventions safer.

The middle cerebral artery (MCA), which is one of the three major arteries supplying the blood flow to the brain, is the largest and the most complex.1–5 One of the areas extensively supplied by this important artery is the temporal region. This is the region that contains the primary and secondary hearing centers known as Heschl’s gyri, the cortical regions of sensory speech area such as Wernicke’s; it is also a region contributing to personality and memory functions.6 Various studies have investigated the feeding of the temporal region by the MCA.7,8 Although the branches of the MCA involved in the feeding of this region have been described,1,9 there is no clear detailed description of the structure of the blood supply from the MCA to the temporal region, and only the temporal artery (TA), which is an important feeder of this region, has been defined and named but not discussed in detail.2 In addition, the TA constitutes the temporal cortical arteries. This study was conducted to describe in detail one of the important feeding areas of the MCA, the temporal region and the blood supply to the temporal region by the MCA and its cortical branches. The aim of this study was to demonstrate, define and describe the clinical importance of the TA, a branch that is often overlooked in the literature and not generally involved in classical cortical arterial distribution.

MATERIALS AND METHODS

This study was conducted at the Surgical Neuroanatomy Laboratory of the Department of Anatomy at Ankara University School of Medicine using a total of 22 human brains (44 hemispheres) without a history of trauma or pathology of the central nervous system. First, both the two internal carotid arteries and the basilar arteries were cannulated in all brains and filled with latex. All dissections were performed by the microdissection technique using microsurgical tools and under the microscope (Zeiss-OPMI, Jena, Germany). All morphometric measurements were conducted by the same team using a caliper with a precision of 0.01 mm. Before dissection, all brains were separated into two hemispheres from the midline. Then, lobectomies of each temporal lobe were performed at the border 5 cm away from the pole. The cortical branches feeding the temporal lobe and their exit patterns from the TA, their relationships with each other and the feeding areas were evaluated.

Statistical analysis of the obtained data was conducted using the SPSS for Windows 11.5 package program. The independent samples t test was used for comparisons of results of two groups, and unidirectional variance analysis and Bonferroni tests were used for comparisons of more than 2 groups.

Arithmetic mean standard deviation is represented as descriptive values.

The statistical significance level was considered as 0.05.

RESULTS

The TA was found to be exiting as an early branch or exiting from a trunk, which was observed in almost every hemisphere, being larger than the other cortical branches and giving rise to minimally 2

cortical branches to feed the temporal region and commonly having a single or sometimes a double structure (Figs. 1A-B). It was observed in all hemispheres, except 2 hemispheres (95%). Regarding TA classification, the following 4 types were identified: Type 0: No TA, cases in which it is never found (4%), Type I: exiting as a single branch and giving rise to two cortical branches (20 hemispheres, 45%) Type II: exiting as a single branch and giving rise to three or more cortical branches (15 hemispheres, 34%) and Type III: double TA, in which it is found as 2 TA branches (7 hemispheres, 16%) (Figs. 2 and 3). Of 49 TAs detected in 44 hemispheres, 37 were found as early branch (75%) and 12 originated from the inferior trunk (IT) (24%). It was observed that the TA never originated from other trunks except the IT. The diameter of the vessel (average: 2.02 mm) was significantly larger when it emerged as the second branch of TA according to the situation when it emerges as the first or single branch (average diameter 1.73 mm). In 37 hemispheres from which the TA originated as an early branch (ETA), it was observed that it originated from the group of Type I in 15 hemispheres, Type II in 13 hemispheres and Type III in 9 hemispheres. The average diameters of the E-TA according to groups were measured as follows: 1.7mm for Type I, 1.71mm

for Type II and 1.76mm for Type III. The average diameter of the TA originating from the early branch was 1.71 mm. In 12 hemispheres from which the TA originated from the IT (IT-TA), it was observed to originate from Type I in 5 hemispheres, Type II in 2 hemispheres and Type III in 5 hemispheres. The average diameters of the IT-TA groups were measured as follows: 1.57mm for Type I, 1.83mm for Type II and 1.94mm for Type III. The average diameter of the TA originating from the IT was 1.77 mm. In general, the average diameters of the arteries were 1.63mm for Type I, 1.86mm for Type II and 1.78mm for Type III. The average diameter of the TA was 1.75mm (Supplementary Digital Content, Tables 1–4, http://links.lww.com/SCS/C519).

The distances between the tips of the arteries were calculated as 1.86 0.12mm for Type I and 1.78 0.22mm for Type III. Based on these data, only the measurement for Type II group was statistically and significantly higher than that for Type I group (P.0.008). There was no statistically significant difference between the tips of E-TA and those of IT-TA (Supplementary Digital Content, Table 3, http://links.lww.com/SCS/C519).

In Type I TA, the 2 cortical branches that originated from the TA were TPA and ATA in 11 hemispheres (55%), ATA and MTA in 5 hemispheres (25%) and MTA and PTA in 4 hemispheres (20%). In 15 hemispheres with Type II TA, the TA gave rise to 3 cortical branches in 11 hemispheres (73%), 4 cortical branches in 2 hemispheres (13%), and 5 cortical branches in 2 hemispheres (13%). When giving rise to a high number of cortical branches, such as 4 or 5, the TA originated as early branch in 3/4 and from the IT in 1/4. In Type III TA, which was observed in 7 hemispheres, 2 cortical branches originated from each TA in 4 hemispheres (57%), 2 cortical branches originated from the first branch of TA and 3 cortical branches originated from the second branch of TA (42%). No other branching pattern different from this pattern was observed for Type III TA (Supplementary Digital Content, Tables 5–7, http://links.lww.com/SCS/C519) (Figs. 1–3).

The temporopolar artery (TPA) was detected in 36 of 44 hemispheres (81%). It emerged as an early branch in 11 hemispheres (30%), from the E-TA in 21 hemispheres (58%) and from the IT-TA in 4 hemispheres (11%). Its diameter was measured as 0.93mmwhen it emerged as an early branch, 0.87mm when it emerged from the ETA and 0.80mm when it emerged from the IT-TA. The average diameter of the TPA was 0.87mm (Supplementary Digital Content, Tables 4 and 8, http://links.lww.com/SCS/C519) (Figs. 1–3).

The anterior TA (ATA) was detected in all hemispheres. It was found to emerge as an early branch in 6 hemispheres (13%), from the E-TA in 30 hemispheres (68%), from the IT-TA in 6 hemispheres (13%) and from the IT in 1 hemisphere (2%). The average diameters were measured as follows: 1.23mm when it emerged as an early branch, 1.18mm when it emerged from the E-TA, 1.06mm when it emerged from the IT-TA and 1.93mm when it originated directly from the IT. The average diameter of the ATA was 1.19mm (Supplementary Digital Content, Tables 4 and 8, http://links.lww.-com/SCS/C519) (Figs. 1–3).

ThemiddleTA(MTA)was also observed in all hemispheres (Video 1 (Anterior and middle temporal arteries originating from TA2. ( :bifurcation of middle cerebral artery, a: Inferior trunk, b: Superiortrunk)), http://links.lww.com/SCS/C520). It was found as an early branch in 3 hemispheres (6%) and originated from the E-TA in 23 hemispheres (52%), from the IT-TA in 8 hemispheres (18%) and from the IT in 10 hemispheres (22%). The average diameters were 1.4mm when it emerged as an early branch, 1.21mm when it originated from the E-TA, 1.24mm when it emerged from the IT-TA and 1.24mm when it directly originated from the IT. In general, the average diameter of the MTA was 1.23mm (Supplementary Digital Content, Tables 4 and 8, http://links.lww.com/SCS/C519) (Figs. 1–3).

The posterior temporal artery (PTA) was detected in all hemispheres (Video 1(Anterior and middle temporal arteries originating from TA2. ( : bifurcation of middle cerebral artery, a: Inferior trunk, b: Superior trunk)), http://links.lww.com/SCS/C520), but it never emerged as an early branch. It originated from the E-TA in 15 hemispheres (34%), from the IT-TA in 7 hemispheres (15%) and from the IT in 22 hemispheres (50%). The average diameters were 1.34mmwhen it emerged from the E-TA, 1.32mmwhen it emerged from the IT-TA and 1.38mm when it directly originated from the IT. In general, the average diameter of the PTA was 1.35mm (Supplementary Digital Content, Tables 4 and 8, http://links.lww.-com/SCS/C519) (Figs. 1–3).

The temporooccipital artery (TOA) was detected in all hemispheres, but it never emerged as an early branch. It originated from the E-TA in 4 hemispheres (9%), from the IT-TA in 3 hemispheres (6%) and from the IT in 37 hemispheres (84%). The average diameters were 1.38mm when it originated from the E-TA, 1.66mm when it emerged from the IT-TA and 1.59mm when it directly originated from the IT. In general, the average diameter of the TOA was 1.63mm (Supplementary Digital Content, Tables 4 and 8, http://links.lww.com/SCS/C519) (Figs. 1–3). There was no statistical difference between the groups of arterial diameters of the TPA, MTA, PTA, and TOA (Supplementary Digital Content, Table 9, http://links.lww.com/SCS/C519).

DISCUSSION

The arterial structures that provide blood supply to the temporal region are known. The posterior cerebral artery and especially the MCA predominate this region.3,8,10 The cortical branches of the MCA in the temporal region can be specified as the TPA, ATA, MTA, PTA and TOA.1–3,8,10,11 The feeding areas of these cortical branches are as follows: the TPA (termed ‘polar tempolar artery’ with reference to the Terminologia Anatomica TA, 1998)12 supplies blood to the temporopolar area that contains the anterior poles of the superior, middle and inferior temporal gyri; the ATA feeds the anterior temporal area that constitutes the anterior region of the superior, middle and inferior temporal gyri; the MTA (termed ‘middle temporal branch’ with reference to the Terminologia Anatomica TA, 1998)12 supplies blood to the middle temporal area that contains the superior temporal gyrus adjacent to the region at the level of the pars triangularis and pars opercularis, the middle part of the middle temporal gyrus and the middle and the posterior regions of the inferior temporal gyrus; the PTA supplies blood to the posterior temporal region that contains the middle and posterior parts of the superior temporal gyrus, one-third posterior part of the middle temporal gyrus and the posterior tip part of the inferior temporal gyrus and finally, the TOA (termed ‘temporooccipital branch’ with reference to the Terminologia Anatomica TA, 1998)12 feeds the temporooccipital area that contains the posterior half of the superior temporal gyrus, the posterior tip parts of the middle and inferior temporal gyri and the inferior part of the lateral occipital gyrus.3 The terminal branches of MCA form the cortical arteries. According to the Terminologica Anatomica, these arteries can be classified as the superior and inferior terminal branches.12 Recently, these terminologies for the central nervous system were revised in the Terminologia Anatomica TA (1998) by the Working Group Neuroanatomy of the Federative International Programme for Anatomical Terminology (FIPAT) of the International Federation of Associations of Anatomists (IFAA), which is available online as the Terminologia Neuroanatomica (TNA, 2017; published online in 2017 and approved by the IFAA General Assembly in 2019; http://FIPAT.library.dal.ca; for an introductory paper, see Donkelaar et al. 2017) as the official FIPAT terminology.13 The updated terminology has been similarly described in the relevant neuroanatomy books according to TNA.14,15 Based on recent clinical literature, these 2 arteries (anterior TA and anterior temporal branch) are indeed the same.1,3,16 Moreover, the anterior temporal, middle temporal, posterior temporal, and temporo-occipital branches of MCA are mentioned, respectively, as anterior temporal, middle temporal, posterior temporal and temporo-occipital arteries in many recent articles and books from the related field.1,3,8,10,16–19

The literature reports detailed studies about the five cortical branches that feed the temporal region.2,3,10 The term ‘early branch’ was used by Crompton who introduced it to identify the branches that emerge before the separation point where the MCA gives rise its original trunks.20 Detailed studies regarding the early branches of the MCA were presented then, and the early branches responsible for the feeding of the temporal area were termed as early temporal branches.1,2,21 Vuillier et al used the term ‘the early cortical branch’ for the early branches emerging from the M1 segment and demonstrated the correlation of these structures with MRI angiographies.22 In the current study, we attempted to describe not only the early branches providing branches to the temporal region but also the presence of the TA, which was previously reported in the literature by our research team and an attempt was also made to describe its types.2 It was observed that the cortical branches that supply blood to the temporal region, whether early or not, originated froma basic arterial structure often termed as the TA. This branch was found to emerge either as an early branch or from the IT of theMCA, and it often had a single but rarely double pattern. TA could be an origin for two to four cortical arterial structures that feed the temporal region. It is clear that there is no trunk structure of TA, but this has not been mentioned in the classical nomenclature. Tanrio¨ver et al also provided a detailed explanation about the cortical arteries of the temporal region and even described the information indicating that these cortical branches can emerge from a more major branch, and they also classified the branching patterns of the cortical branches.1 Although the configuration of the cortical arteries of the temporal region and the arterial structures from which they could originate were illustrated through figures along with a detailed explanation in their study, those structures were not named. We focused on the TA, which is the major arterial structure in the cortical branch form.Weestablished the definition and the branching patterns by classification. In a study pertaining to the emerging patterns of temporal region arteries, it was reported that the TPA, ATA, MTA, PTA, and TOA originated from the E-TA at proportions of 40%, 30%, 18%, 7% and 4%, respectively.1 In the present study, these rates were 58%, 68%, 52%, 34%, and 9%, respectively, and similar data were obtained in our previous study on this subject.2 In the present study, the arterial diameters of Type II TA according to our classification were found to be significantly larger than those of other types. For Type II, it was believed that giving rise to three or more cortical branches was the reason for the larger arterial diameter. When the exit points of TA were examined, it was observed that the arterial diameters were large when it exited from the E-TA in Type II and from the IT-TA in Type III, and the diameters were smaller in Type I IT-TA according to other exiting locations. The ET-TAs were primarily giving rise to cortical branches in the temporal region. The two cortical branches in Type I were detected as TPA.ATA. It was also observed that when it gave rise to multiple branches in Type II, it was mostly giving rise to triple branches. In Type III, the cortical branch distribution of TA was mostly formed by giving rise to two branches from each TA. The largest of the temporal cortical branches was the TOA and the smallest was the TPA.

Grivas et al23 reported about the post-operative intracerebral hemorrhage phenomenon in their study based on the results of 52 patients over the age of 50 years who were operated for refractory epilepsy. There was a possibility of the development of complications associated with the arteries in the temporal region while performing the temporal lobectomy/lesionectomies and amygdalohippocampectomy procedures in the epilepsy surgery of the temporal region. Further information about the temporal region arteries is thus expected to decrease the occurrence of these complications. In another study, Clusmann et al24 described postoperative hemorrhage in 17 of 442 patients operated for the temporal lobe epilepsy, wherein 3 of 4 patients with post-operative intra-axial hematoma became critical. Therefore, arterial injuries recorded in the etiology of intra-axial hematoma were found to be associated with a high rate of mortality and morbidity. Thus, adequate knowledge about vascular anatomy and the distribution patterns of arteries play an important role in decreasing this type of complications. Another study25 warned about such complications, where four patients developed a stroke in this area during surgery of the left posterior temporal lobe after craniotomy. In addition, Briggs et al25 reasoned that this complication, wherein speech mapping was rendered impossible due to ischemia, results from decreased flow in the distribution of a posterior temporal branch of the MCA. Accordingly, the reason ‘the artery of aphasia’ was considered a hypothesized vascular territory of approximate locations of the relevant portions’ courses over the lateral surface of the superior temporal gyrus near the bend of the Sylvian fissure. Moreover, the disruption of this artery can cause receptive and expressive language deficit. Based on the findings of the present study, this area is supplied by a posterior TA and the TOA. Therefore, ‘the artery of aphasia’ can be explained more comprehensively with these two arteries. The knowledge about the anatomical distribution patterns of these two cortical arteries is expected to minimize the development of complications associated with operations, such as aphasia and language-speech problems.

Knowledge of the blood supply pattern of the temporal region is undoubtedly important, especially in the presence of lesions and vascular pathologies in this region, as it also involves the Wernicke’s area.23,26–29 Several researchers have reported that the postoperative visual field defects, verbal memory dysfunctions, severe amnesia and hemorrhagic complications that may lead to death can be observed with surgical procedures of this region.23,24,30–32 Briggs et al termed the PTA as ‘artery of aphasia’ in cases with verbal deficits observed after surgery according to infarct of the PTA.25 Although it rarely occurs in the distal segments of the TAs, especially in the presence of aneurysms of the TA branches that emerge as early branches, the neurovascular anatomical information of these structures is even more important.33–35 The cortical branching arteries of this region, such as the TPA, ATA, and MTA, can also be proposed as a model for revascularisation-bypass operations.36–40

This study was performed on isolated hemispheres; therefore, it was not possible to obtain data regarding the sex and age of the donors. Additionally, only specimens that permitted adequate dissection and assessment of morphology to demonstrate the branching pattern of arteries were selected; therefore, the number of specimens with intact and filled arteries available for dissection and to demonstrate relationships was another limitation.

In conclusion, this study demonstrated the temporal region supplied by the branches of the MCA, which is one of the important regions of the brain. When the feeding pattern of this region was examined, the TA was observed in detail to be an important anatomical structure originating from the cortical branches present here. We believe that the knowledge of the existence and properties of these arterial structures will reduce the possibility of complications in surgical procedures in this region, thereby providing safer and successful surgeries.

ACKNOWLEDGMENTS

The authors thank Mr Goksel Erkal for creating the illustrations. In addition, the authors thank all donors who donated their bodies for anatomical study and research of the cadaver brains used in this study and their families.

REFERENCES

1. Tanriover N, Kawashima M, Rhoton AL, et al. Microsurgical anatomy of the early branches of the middle cerebral artery: morphometric analysis and classification with angiographic correlation. J Neurosurg 2003;98:1277–1290

2. Kahilogullari G, Ugur HC, Comert A, et al. The branching pattern of the middle cerebral artery: is the intermediate trunk real or not? An anatomical study correlating with simple angiography. J Neurosurg 2012;116:1024–1034

3. Rhoton AL Jr. The supratentorial arteries. Neurosurgery 2002;51(Suppl 4):53–120

4. Cilliers K, Page BJ. Anatomy of the middle cerebral artery: Cortical branches, branching pattern and anomalies. Turk Neurosurg 2017;27:671–681

5. Ogeng’o JA, Njongo W, Hemed E, et al. Branching pattern of middle cerebral artery in an African population. Clin Anat 2011;24:692–698

6. Fitzgerald MJT, Folan-Curran J. Clinical neuroanatomy and related neuroscience. Fourth Edition. Edinburgh London: WB Saunders; 2002:, 241-253

7. DeLong WB. Anatomy of the middle cerebral artery: the temporal branches. Stroke 1973;4:412–418

8. Gibo H, Carver CC, Rhoton AL Jr et al. Microsurgical anatomy of the middle cerebral artery. J Neurosurg 1981;54:151–169

9. Baskaya MK, Coscarella E, Tummala RP, et al. Surgical management of middle cerebral artery aneurysms: surgical anatomy, approaches and pitfalls. Neurosurg Q 2005;15:201–210