RAMIFICATIONS OF THE MIDDLE CEREBRAL ARTERY IN POLAR FOX (ALOPEX LAGOPUS)
DOI:10.30825/5.EJPAU.27.2017.20.3

Benedykt Skoczylas, Witold Brudnicki, Krzysztof Kirkiłło-Stacewicz, Włodzimierz Nowicki, Jan Wach
Department of Animal Physiology, Zoophysiotherapy and Feeding, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Bydgoszcz, Poland

ABSTRACT

The studies of the vascularization of the cerebrum in polar fox were performed on 80 cerebral hemispheres. It was found that the middle cerebral artery is the strongest vessel supplying blood to the cerebrum. The artery gets divided into ten permanent branches. Two olfactory arteries supply the region of the cerebrum located on the border between the old and the new cortex. The other eight get divided into three branches running towards the region of frontal lobe of the brain, two branches to the region of the parietal lobe and three temporal branches running in the temporal region, which supply blood only to the new cortex of the cerebrum. The frontal, parietal and temporal branches descended independently from the main trunk of the middle cerebral artery or formed a common trunk. Common trunks for respective groups of branches have been described as the rostral, dorsal and caudal middle cerebral artery. In 10% of the cases there occurred two independent branches of the middle cerebral artery from the rostral cerebral artery.

Key words: cerebrum, vascularization, polar fox.

INTRODUCTION

The first information on the anatomy of the middle cerebral artery of various mammalian species is reported by Hoffman [5]. More through data on the anatomy of the middle cerebral artery in dog and its branches have been described by Habermehl [4]. The author only dealt with the anatomy of that artery and described the topography of its branches on the surface of the cerebrum and disregarded its variation completely. In literature there appeared the reports which describe in detail the cortical branches of the middle cerebral artery. The issues have been described in cat by Chadzypanagiotis [3] in which the author provides nomenclature on respective cortical branches of that artery. Systematized descriptions of the anatomy and the pattern of cortical branches of the middle cerebral artery in some Carnivora species are described by Wiland [14]. Over the last years there appeared numerous reports on the anatomy of the middle cerebral artery in different mammalian species, which refers to the vessels that are distinguished as single branches e.g. in silver fox [9], in cattle [10], in fallow deer [11], in otter [12] and multiple arteries that occur in wild boar [8], in domestic pig [7]. In the papers it was found that the cortical branches of the middle cerebral artery in those animal species reach the same regions of the cerebrum. The differences occur in the pattern of descent and division of respective cortical branches of the middle cerebral artery. The pattern of division of the middle cerebral artery is affected by how the species has been classified and the pattern of groove-coverage of the cortex [1]. In mammals on the surface of the cortex there is a different pattern of sulci, which can affect the structure of the cortical branches of the middle cerebral artery. In the vast literature there seem to be missing a paper on the cortical branches of the middle cerebral artery in polar fox. In that species Wiland [13,14] described the anatomy and variation in the arteries of the base of the brain. Considering the discrepancy resulting from respective descriptions and considering new studies, one has decided to investigate the pattern, the division and variation of cortical branches of the middle cerebral artery in polar fox and to compare the results with the data reported by other authors.

MATERIAL AND METHODS

The research was performed on 40 brains in polar fox of both sexes (20 males and 20 females), namely a total of 80 cerebral hemispheres received from a fox farm at Łachowo. Foxes were one year old. Ethics approval was not required – animals died because of natural reasons. The animal heads were cut off at the height of the 3rd–4th cervical vertebrae. The arteries have not been rinsed and were filled with latex NB 30–60 (89% of latex, 10% of H2O and 1% of black pigment) introduced with medical syringe into the common carotid artery. The heads were fixed in a 5% formalin solution with the cranium closed and parietal bone breached. Then heads were decalcified in hydrochloric acid, the skull cavity was opened and brains were taken out. The cerebral hemispheres were photographed with Nikon DX 90 and the following were being described: the anatomy, the division pattern and the course of cortical branches of the middle cerebral artery.

RESULTS

In polar fox the blood is supplied to the brain with internal carotid arteries and vertebral arteries (Fig. 1).

Fig. 1. Blood supply to the brain by brain base arteries in polar fox 1 – Internal carotid artery, 2 –Vertebral artery

The common carotid artery, having entered the skull cavity and penetrated the dura mater, bifurcates into the rostral cerebral artery and caudal communicating artery which, together with their symmetrical vessels form an arterial circle of the brain. From the initial section of the rostral cerebral artery towards the cortex there separates the middle cerebral artery.

The middle cerebral artery is the strongest vessel supplying blood to the cerebrum. The initial section of the main trunk of the middle cerebral artery goes along the dorsal surface of the optic tract. Then the section gets bended around the piriform lobe and goes through its rostral margin. Further on it runs to the lateral olfactory sulcus and, having passed it, it gets divided. From the initial section of the main trunk of the middle cerebral artery there descend minor central branches supplying blood to olfactory tracts and the piriform lobe. The main trunk of the middle cerebral artery gets divided into a number of cortical branches which run to the specific region of the cerebral hemisphere, supplying blood to specific regions of the brain.

The first permanent branches of the middle cerebral artery which supply both the old and the new cortex are olfactory arteries.

The rostral olfactory artery (Fig. 2-1), having separated from the main trunk of the middle cerebral artery, runs to the rostral part of the lateral olfactory sulcus it can ascend into in various places. Its terminal branches can also appear again from under the lateral olfactory sulcus and then ascend under the cortex surface.

Fig. 2. Diagram of the division of the middle cerebral artery on the surface of the cortex in polar fox 1 – Rostral olfactory artery, 2 – Caudal olfactory artery, 3 – Orbital branch, 4 – Ventral frontal branch, 5 – Dorsal frontal branch, 6 – Rostral parietal branch, 7 – caudal parietal branch, 8 – dorsal temporal branch, 9 – middle temporal branch, 10 – ventral temporal branch, a – internal carotid artery, b – rostral cerebral artery, c – caudal communicating artery, d – Sylvian fissure, e – Presylvian sulcus, f – rostral lateral olfactory sulcus, g – caudal lateral olfactory sulcus, h – rostral Suprasylvian sulcus, i – middle Suprasylvian sulcus, j – caudal Suprasylvian sulcus, k – rostral ectomarginal Sylvian sulcus, l – middle ectomarginal Sylvian sulcus, m – caudal ectomarginal Sylvian sulcus, n – ansiform sulcus, o – marginal sulcus, p – ectomarginal sulcus, r – coronary sulcus.

The caudal olfactory artery (Fig. 2-2) ascends into the caudal part of the lateral olfactory sulcus and its terminal branches supply the area of the cortex found under the sulcus.

The other branches of the middle cerebral artery supply the areas of the cortex over the lateral olfactory sulcus. On the cortex towards the frontal lobe there spread three thick branches. As the first one there separates the orbital branch (Fig. 2-3) which is located lowest and it goes towards the region of the Presylvian sulcus where its terminal branches reach the coronary groove.

The ventral frontal branch (Fig. 2-4) vascularizes the middle part of the frontal lobe. The vessel goes through the rostral ectomarginal Sylvian sulcus and the rostral Suprasylvian sulcus towards the coronary groove it passes towards the fornix.

The dorsal frontal branch (Fig. 2-5), having separated from the middle cerebral artery at the height of the rostral ectomarginal Sylvian sulcus, goes up to the region of the cruciate sulcus. The vessel supplies blood to the upper part of the medial surface of the frontal lobe.

The next vessel which runs towards the parietal lobe bifurcates into two branches.

The rostral parietal branch (Fig. 2-6) runs towards the middle ectomarginal Sylvian sulcus to the marginal sulcus. The terminal twigs of that vessel supply blood to the area of the cortex found under the ansiform sulcus.

The caudal parietal branch (Fig. 2-7) also runs to the region of the marginal sulcus and further on it branches out into smaller vessels. Some of them ascend into the medial Suprasylvian sulcus.

The lateral-posterior surface of the cerebral hemisphere is supplied by the branches of the middle cerebral artery which descend from at various heights and they are referred to as  temporal branches.

The dorsal temporal branch (Fig. 2-8) is usually the strongest cortical branch of the middle cerebral artery and its further continuation in the area of the cortex. Having left the Sylvian fissure, it runs towards the middle Suprasylvian sulcus and further to the upper margin of the cerebral hemisphere. The branch supplies blood to the upper part of the cortex.

The middle temporal branch (Fig. 2-9) descends a small distance away from the previous branch. The branches of that vessel spread towards the ectomarginal sulcus. Its terminal branches go onto the surface of the occipital lobe.

The ventral temporal branch (Fig. 2-10) runs to the end of the caudal ectomarginal Sylvian sulcus. Having passed the posterior part of the sulcus, its branches spread towards the caudal Suprasylvian sulcus. Its terminal branches take part in the supply of a part of the occipital lobe.

Considering the general pattern of the spread the cortical branches of the middle cerebral artery in polar fox, one shall note that respective sections of those branches can run inside respective sulci, sometimes undergoing further divisions, always running towards the cortex areas described. Analysing the pattern of descent of the cortical branches of the middle cerebral artery in the polar fox individuals investigated, it was found that from the rostral cerebral artery on 72 cerebral hemispheres there descended a single independent vessel; the middle cerebral artery. Among them on 12 (15%) hemispheres from the main trunk of the middle cerebral artery there descended rostrally a common trunk for the rostral olfactory artery and for the orbital branch, then a common descend from the ventral and dorsal frontal branches. The main trunk caudally gave rise to the caudal olfactory artery with a common descent with the rostral temporal branch. Having ascended into the Sylvian fissure, on the surface of the cortex it showed a common trunk for rostral and caudal parietal branches as well as for the middle and dorsal temporal branches.

In another 14 (17.5%) cases there descended rostrally an independent rostral olfactory artery and a common trunk for the orbital, rostral and dorsal frontal branches. The main trunk got onto the surface of the cerebral cortex from the Sylvian fissure and formed a common descent for rostral and caudal parietal branches. Caudally from the main trunk of the middle cerebral artery, with a common trunk there separated the dorsal, middle and ventral temporal branches, whereas the caudal olfactory artery got separated independently from the main trunk of the middle cerebral artery (Fig. 3). On another 10 (12.5%) hemispheres from the main trunk the following separated rostrally with a common trunk: the orbital branch, the ventral frontal branch and the rostral olfactory artery. The main trunk of the middle cerebral artery, having got into the surface of the cortex, separated a common descent for the dorsal frontal branch and rostral and caudal parietal branches. Caudally from the main trunk the following separated with a common descent: the ventral, middle and dorsal temporal branches as well as an independent caudal olfactory artery.

Fig. 3. Division of the middle cerebral artery into the rostral middle cerebral artery – A, from which there descend the following: orbital branch – 3, ventral frontal branch  – 4,  and dorsal frontal branch – 5, into the dorsal middle cerebral artery – B, from which there descend the parietal branches: rostral – 6, caudal – 7 as well as into the caudal middle cerebral artery – C, from which there descend the following branches: temporal: dorsal – 8, middle – 9 and ventral  – 10. Rostral olfactory artery – 1, Caudal olfactory artery – 2 – descend independently from the main trunk of the middle cerebral artery.

In 14 (17.5%) cases from the main trunk there descended rostrally independently the rostral olfactory artery, then a common descent for the orbital branch and for the ventral and dorsal frontal branches. Caudally from the main trunk there separated, with a common descent, the middle and ventral temporal branches as well as the caudal olfactory artery. The main trunk, having ascended into the Sylvian fissure, got onto the surface of the cortex with a common descent for rostral and caudal parietal branches and the dorsal temporal branch.

On yet another 12 (15%) cerebral hemispheres from the main trunk rostrally there separated, with a common descent, the orbital branch, ventral and dorsal frontal branches with the rostral olfactory artery. Caudally from the main trunk of the middle cerebral artery the following separated with a common descent: the rostral and caudal parietal branches as well as temporal branches: the dorsal, middle and caudal ones. The caudal olfactory artery descended independently from the main trunk. In another 10 (12.5%) cases from the main trunk there descended rostrally a common descent for the rostral olfactory artery, the orbital branch and the ventral frontal branch. A common trunk for the ventral temporal branch and caudal olfactory artery constituted a caudal branch. The main trunk, having ascended into the Sylvian fissure, got onto the cortex surface with a common descent for the dorsal frontal branch, rostral and caudal parietal branches and dorsal and middle temporal branches.

On the other 8 (10%) hemispheres it was found that from the rostral cerebral artery there bifurcated two independent branches of the middle cerebral artery. Among them in 4 (5%) cases the first independent branch from the rostral cerebral artery was the rostral olfactory artery, while the second branch from the rostral cerebral artery – the main trunk of the middle cerebral artery from which there descended rostrally independently: the orbital branch and the caudal frontal branch. Caudally from the main trunk there separated an independent caudal olfactory artery and a common descent of the ventral and middle temporal branches. The main trunk, having descended into the Sylvian fissure, got onto the surface of the cortex with a common descent for dorsal frontal, rostral and caudal parietal branches as well as dorsal temporal branch.

On yet another 2 (2.5%) brains from the rostral cerebral artery there descended independently the caudal olfactory artery. Rostrally from main trunk there independently separated the rostral olfactory artery, the orbital branch, the ventral frontal branch, the dorsal frontal branch, successively. Caudally from the main trunk there descended an independent ventral temporal branch. The main trunk, having ascended into the Sylvian fissure, got onto the cortex surface with a common descent for rostral and caudal parietal branches as well as dorsal and middle temporal branches. In the other 2 (2.5%) cases the first independent descent from the rostral cerebral artery was a common trunk for the rostral olfactory artery and the orbital branch. The other independent descent from the rostral cerebral artery was the main trunk of the middle cerebral artery from which, rostrally and independently there separated the ventral and dorsal frontal branches. Caudally from the main trunk there separated independently the caudal olfactory artery, a common descent for the ventral and middle temporal branches. The main trunk, having ascended into the Sylvian fissure, got onto the cortex surface with a common descent for the rostral and caudal parietal branches as well as the dorsal temporal branch.

DISCUSSION

The middle cerebral artery supplies blood to the greatest region of the cerebrum and of all the vessels it is the best developed branch. In the polar fox the middle cerebral artery supplies the same areas of the brain as in the mammalian species studied so far. The discrepancies concern mostly its division into respective branches. Chadzypanagiotis [3], describing the cortical branches in cat, differentiated between the branches supplying the old cortex, the branches on the border of the old and the new cortex as well as the branches for the new cortex. In the polar fox the arteries supplying the old cortex are minor branches onto the piriform lobe and olfactory tracts. On the border of the old and the new cortex there are found the rostral and caudal olfactory arteries. In the polar fox the rostral olfactory artery in 5% of the cases was a vessel which descended independently from the rostral cerebral artery. On the other cerebral hemispheres it was a vessel which got separated independently from the main trunk of the middle cerebral artery in 37.5% of the cases. In 17.5% of the cases it formed a common descent with the orbital branch. On the 25% of the cerebral hemispheres it was one of the branches descending from the common trunk of the middle cerebral artery which gave rise to the orbital branch and the ventral frontal branch.

In the other 15% cases the rostral olfactory artery demonstrated a common descent with the orbital, ventral and dorsal frontal branches.

The caudal olfactory artery, on the other hand, in 2.5% of the cases was a vessel which descended independently from the rostral cerebral artery. On 52.5% hemispheres it was the vessel descending independently from the main trunk of the middle cerebral artery. In 27.5% of the cases the caudal olfactory artery separated with a common descent with the ventral temporal branch. In the other 17.5% hemispheres it was one of the branches of a common trunk for ventral and middle temporal branches.

The other cortical branches of the middle cerebral artery can be divided into a group of frontal, parietal and temporal branches. In the polar fox, similarly as in other Carnivora species there occur eight main vessels which supply blood to the area of the new cortex of the cerebrum.

Besides, respective cortical branches can descend from the main trunk of the middle cerebral artery with a common descent. Such cases of descent were reported by Chadzypanagiotis [3], Wiland [16], Skoczylas et al. [12] as the rostral, dorsal and caudal middle cerebral artery. In polar fox the anterior middle cerebral artery has been presented as a common trunk for frontal branches and it occurred in 35% of the cases investigated, the dorsal middle cerebral artery was described as a common trunk for parietal branches, which was observed in 17.5% of the cases. The caudal middle cerebral artery as a common trunk for temporal branches was found in 30% of the cases.

In polar fox the dorsal middle cerebral artery occurred as the lowest percentage of the cases, however, here the rostral middle cerebral artery dominated. Making a comparison of the present results with those reported by Wiland [16], one can state that also in American mink the dorsal middle cerebral artery was reported as the lowest percentage of the cases. In polar fox, similarly as in the other animal species studied, the parietal branches have developed poorest. On the surface of the cerebrum the best developed are the frontal branches of the middle cerebral artery.

From the description of the structure of the middle cerebral artery in the publications by Jabłoński et al. [6], Skoczylas et al. [11, 12] in yellow grivet, fallow deer and European otter one can see that it is usually a single vessel descending from the rostral cerebral artery. The vessel, having passed the lateral olfactory sulcus, gets divided along its course into respective cortical branches. In the material investigated such a pattern of division of the middle cerebral artery was found in 90.0% of the cases. In polar fox there were identified the cases of descent from the rostral cerebral artery of two independent arterial trunks in 10% of the cases. The second independent branch from the rostral cerebral artery was the rostral olfactory artery in 5% of the cases, the caudal olfactory artery – 2.5% of the cases and a common trunk of the rostral olfactory artery with the orbital branch in 2.5% of the cases. In other mammalian species the presence of two independent descents of the branches of the middle cerebral artery was found in domestic rabbit in 31.4% [15], in wild rabbit [2] in 36.5% of the cases.

The present research show that in polar fox the observed division of the middle cerebral artery into the same branches or their groups, like in the other mammalian species investigated so far is a result of genetic limitations.

CONCLUSIONS

1. The middle cerebral artery supplies blood to the greatest region of the cerebrum and of all the vessels it is the best developed branch.
2. In polar fox the dorsal middle cerebral artery occurred as the lowest percentage of the cases.
3. The first permanent branches of the middle cerebral artery which supply both the old and the new cortex are olfactory arteries.

REFERENCES

1. Brauer K. & Schaber W., 1970. Katalog der Säugetiergehirne. VEB Gustaw Fisher Verlag Jena.
2. Brudnicki W., Nowicki W., Skoczylas B., Brudnicki A., Kirkiłło-Stacewicz K., Wach J., 2012. Arteries of the brain in wild European rabbit Oryctolagus cuniculus (Linnaeus, 1758). Folia biologica, 60 (3–4), 189–194.
3. Chadzypanagiotis D., 1975. Arteries on the surface of the cerebral hemisphere in the cat. Folia Morphologica, Warsaw, 32, 385–399.
4. Habermehl K.H., 1973. The topography of blood vessels in dogs. Anatomia Histologia Embryologia, 2, 327–353.
5. Hofmann M., 1900. Zur vergleichenden Anatomie der Gehirn und Ruckenmarksarterien der Vestebraten, Zeitschrift fur Morphologie und Anthropologie, 2, 247–320.
6. Jabłoński R., Skoczylas B., Brudnicki W., Nowicki W., 2005. Cortical branches of the middle cerebral artery in grivet (Cercopithecus aethiops). Prace Komisji Nauk Rolniczych i Biologicznych, BTN, B, 56, 51–55.
7. Skoczylas B., 2000. Cortical branches of middle cerebral artery in domestic pig (Sus scrofa f.domestica). EJPAU, Veterinary Medicine Series, Vol. 3, Issue 1.
8. Skoczylas B., Wiland C., 1999. Cortical branches of the middle cerebral artery in the wild boar (Sus scrofa L.). Electronic Journal of Polish Agricultural University, Veterinary Medicine Series, Vol. 2, Issue 1–6.
9. Skoczylas B., Brudnicki W., Kirkiłło-Stacewicz K., Nowicki W., Wach J., 2016. Cortical branches of the middle cerebral artery in silver fox (Vulpes vulpes). Pesquisa Veterinária Brasileira, 36 (10), 1053–1057.
10. Skoczylas B., Brudnicki W., Kirkiłło-Stacewicz K., Nowicki W., Wach J., 2016. Arterial supply of the cerebral cortex in cattle (Bos primigenius f. dom.). Slovenian Veterinary Research, 53 (1), 13–18. 
11. Skoczylas B., Brudnicki W., Nowicki W., Jabłoński R., Kirkiłło-Stacewicz K., Wach J., 2011. Cortical branches of the middle cerebral artery in fallow deer (Dama dama). EJPAU,  Veterinary Medicine Series, volume14/issue 4/art-09.
12. Skoczylas B., Brudnicki W., Nowicki W., Kirkiłło-Stacewicz K., Jabloński R., Wach J., 2012. The cortical branches of the middle cerebral artery in the otter (Lutra lutra). Veterinarni Medicina, vol. 57, no 6, 282–286.
13. Wiland C., 1965. Variations of the arterial system of the brain basis in polar fox. WSR Annuals, Poznań, 25, 197–206.
14. Wiland C., 1967. Range of variation of the arterial system of the brain basis in polar fox. WSR Annuals, Poznań, 36, 215–231.
15. Wiland C., 1968. Basilar arteries oft he brain in the domestic rabbit. Folia Morphologica, 27, 3, 288–295.
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Accepted for print: 16.09.2017

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Benedykt Skoczylas
Department of Animal Physiology, Zoophysiotherapy and Feeding, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Bydgoszcz, Poland
Bernardyńska 6
85-029 Bydgoszcz
Poland
email: anat@utp.edu.pl

Witold Brudnicki
Department of Animal Physiology, Zoophysiotherapy and Feeding, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Bydgoszcz, Poland
Bernardyńska 6
85-029 Bydgoszcz
Poland
email: anat@utp.edu.pl

Krzysztof Kirkiłło-Stacewicz
Department of Animal Physiology, Zoophysiotherapy and Feeding, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Bydgoszcz, Poland
Bernardyńska 6
85-029 Bydgoszcz
Poland
email: krzysztof.stacewicz@o2.pl

Włodzimierz Nowicki
Department of Animal Physiology, Zoophysiotherapy and Feeding, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Bydgoszcz, Poland
Bernardyńska 6
85-029 Bydgoszcz
Poland
email: wlodek_novika@interia.eu

Jan Wach
Department of Animal Physiology, Zoophysiotherapy and Feeding, Faculty of Animal Breeding and Biology, UTP University of Science and Technology, Bydgoszcz, Poland
Bernardyńska 6
85-029 Bydgoszcz
Poland
email: janwach82@poczta.onet.pl

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