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The rostral epidural rete mirabile of the llama as a place of retrograde transport of various substances – anatomical basics

The rostral epidural rete mirabile of the llama as a place of retrograde transport of various... The aim of this study was to analyse the structure of the rostral epidural rete mirabile in the llama. Some specimens were prepared by injecting stained chemically cured acrylic into the bilateral common carot- id arteries. After about 1 month received vascular corrosion casts on the bone scaffold. Some specimens made using red and blue latex introduced into the bilateral common carotid arteries and the bilateral external jugular vein. The rostral epidural rete mirabile is a well-developed, bilateral structure composed of numerous arteries, which are multiply anastomosed with each other. The cranial section of the rete is asymmetrical. Its lateral part is much better developed, because there are rostral branches to the rostral epidural rete mirabile at this point. The arterial vessels are not accompanied by homonymous veins. How- ever, the arteries of the rostral epidural rete mirabile are accompanied by venous vessels of the cavernous sinus. That rete plays an important role in selective brain cooling, the conservation of body water, and ret- rograde transport of neurotransmitters. CO, GnRH, beta-endorphin, progesterone, testosterone, oxytocin, LHRH and dopamine diffuse from the venous blood of the cavernous sinus to the arterial blood of the ros- tral epidural rete mirabile. Running title: The rostral epidural rete mirabile of the llama Keywords: carbon monoxide, even-toed ungulates, neurotransmitters, RERM Department of Basic and Preclinical Sciences, Institute of Veterinary Medicine, Nicolaus Copernicus University in Toruń, Toruń, Poland *Correspondence: maciejzdun@umk.pl Full list of author information is available at the end of article 106 Zdun et al. Medical Journal of Cell Biology (2021) the blood vessels on the tissues of individual ani- Introduction mals. The names of the anatomical structures were The arterial system of the head of even-toed standardised according to the Nomina Anatomica ungulates is characterised by the presence of the Veterinaria [12]. rostral epidural rete mirabile. Due to the location of this rete in the cavernous sinus, it plays an im- portant role in selective brain cooling [1-3], the Results conservation of body water [4], and retrograde Blood reaches the rostral epidural rete mirabile transport of neurotransmitters [5, 6]. The Artiodac- (rete mirabile epidurale rostrale) through the pa- tyla order (even-toed ungulates) includes numero- ired common carotid artery (arteria carotis commu- us species of animals inhabiting almost all climatic nis) and the external carotid artery (arteria carotis zones of our planet, which can adapt to various externa), which is an extension of the former vessel. environmental conditions, e.g. animals of the Came- The internal carotid artery (arteria carotis interna) liformes, Ruminantia, and Suiformes suborders [7]. branches off in the place where the common carotid The construction of the rostral epidural rete mirabi- artery becomes the external carotid artery. le in selected representatives of ruminants has been The internal carotid artery passes through the well described [8]. Numerous authors describing jugular foramen and joins the rostral epidural rete the vessels of the encephalon base in Cameliformes mirabile. Moreover, this rete is composed of nume- mentioned the rete [9, 10], but did not describe it rous rostral branches to the rostral epidural rete in detail. There has been a description of the mor- mirabile (rami rostrales ad rete mirabile epidurale phometric characteristics of the rostral epidural rostrale) and the caudal branch to the rostral epi- rete mirabile of the dromedary – a representative of dural rete mirabile (ramus caudalis ad rete mirabi- the Old World camelids [11], but this structure has le epidurale rostrale). The rostral branches branch not been described in any representative of the New from the maxillary artery (arteria maxillaris) and World camelids. Each of the suborders of even-toed the external ophthalmic artery (arteria ophthalmi- ungulates differs in the structure of the rostral epi- ca externa). The caudal branch was very thin and it dural rete mirabile. was lacking from one specimen bilaterally and one As there have been numerous scientific publi- specimen unilaterally. cations on the functional nature of this vascular The rostral epidural rete mirabile is a well-develo- region in species of the Ruminantia and Suiformes ped, bilateral structure located on the corpus of the suborders, the aim of this study was to analyse the basisphenoid bone, on the lateral sides of the hypo- structure of the rostral epidural rete mirabile in physial fossa (Fig. 1). It is composed of numerous the llama – a representative of the Cameliformes arteries, which are multiply anastomosed with each suborder. This study may be useful for physiologi- other. The shape of the rostral epidural rete mirabile cal examinations of other suborders of even-toed resembles an elongated oval. The cranial section of ungulates. the rete is asymmetrical. Its lateral part is much bet- ter developed, because there are rostral branches to Material and methods the rostral epidural rete mirabile at this point. At the The study was conducted on 5 specimens of the half-length of the cross-section of the rostral epidu- llama of the Llama subfamily, Cameliformes subor- ral rete mirabile its shape is the most similar to an der. The research material was collected from priva- oval and the rete is composed of tiny vessels of simi- te breeders posthumously. lar diameters. The bilateral retes were connected by Three specimens were prepared by injecting numerous vessels in the caudal section. The number stained chemically cured acrylic DURACRYL PLUS of vessels in the rete ranged from 48 to 61. (SpofaDental, Jičí�n) into the bilateral common ca- The rostral cerebral artery (arteria cerebri rostra- rotid arteries. The specimens were cured after abo- lis) and the caudal communicating artery (arteria ut 20 min. Next, the material was enzymatically ma- communicans caudalis) emerge from the rete. These cerated with Persil powder (Henkel, Düsseldorf ) at vessels are the main arteries forming the cerebral 42°C for about 1 month. The procedure resulted in arterial circle (circulus arteriosus cerebri). vascular corrosion casts on the bone scaffold. Two The arterial vessels are not accompanied by specimens were prepared with another method. homonymous veins. However, the arteries of the Liquid LBS 3060 red latex was introduced into the rostral epidural rete mirabile are accompanied by bilateral common carotid arteries. Moreover, liquid venous vessels of the cavernous sinus (sinus caver- blue latex was introduced into the bilateral exter- nosus). The rostral epidural rete mirabile is embed- nal jugular vein. Next, the material was immersed ded in the cavernous sinus. There are numerous in a 5% formalin solution, where it hardened after small spaces, resulting in a spongy structure of this 7 days. Next surgical instruments were used to ma- sinus. These spaces are filled with vessels of the nually dissect the arteries and to obtain images of rostral epidural rete mirabile. 107 Zdun et al. Medical Journal of Cell Biology (2021) FIGURE 1 Corrosion cast of the rostral epidural rete mirabile 1- rostral epidural rete mirabile 1’ – rostral part of the rete mirabile with rostral branches to the rete 2 – internal carotid artery 3 – caudal branch to the rete mirabile Discussion Bourke [18] also concluded that the rostral epidural The internal carotid artery is one of the vessels rete mirabile was structurally incapable of reducing supplying blood to the rostral epidural rete mirabile the pressure of blood flowing to the brain. Regard- in Cameliformes. It has been described in the Bac- less of whether the rete regulates the flow of blood trian camel, dromedary, llama, and guanaco [9-11]. to the brain or not, many authors see its physiolo- The maxillary artery, which is a direct extension of gical role in the selective brain cooling mechanism. the external carotid artery, splits into the caudal This mechanism was described by Hayward and branch to the rostral epidural rete mirabile and the Backer in 1969 [1]. Its essence is to cool the warmer rostral branches to the rete. The rostral branches blood flowing through the arteries to the brain. The- to the rete branching from the maxillary artery and se arteries form a vast pool in numerous vessels of the external ophthalmic artery are the main vessels the rete washed by cooler blood returning from the supplying blood to the rete in Cameliformes [9-11]. nasal cavity and flowing through the cavernous si- Apart from that, there is a weak caudal branch to nus [1-3, 13]. As a result, during muscular effort the the rostral epidural rete mirabile, which Al Aiyan et animal can maintain the temperature of its brain at al. defined as the middle meningeal artery [10]. 40.5°C. Research conducted on Dorper sheep also A cross-section of the rostral epidural rete mi- proved the importance of selective brain cooling for rabile revealed a bundle of tiny vessels of similar the conservation of body water [19]. diameter. According to Simoens et al. [13], the rete Apart from that, the rostral epidural rete mirabi- has a bipolar structure. Researchers have been in- le together with the cavernous sinus are responsi- terested in the function of this rete for a long time. ble for the retrograde transport of neurotransmit- According to some authors, the rostral epidural rete ters, which is a lesser-known fact. Studies on pigs mirabile regulates the blood flow [14]. However, and sheep have shown that there is GnRH, beta-en- Dieguez et al. [15-17] observed that the arteries dorphin, progesterone or testosterone [5], oxytocin forming the rete did not respond to adrenergic sti- [20], and dopamine [21, 22] diffusion from the veno- mulation and concluded that they did not actively us blood of the cavernous sinus to the arterial blood regulate the flow of blood to the brain. O’Brien and of the rostral epidural rete mirabile. Arterial blood 108 Zdun et al. Medical Journal of Cell Biology (2021) Conflict of interest statement is not mixed with venous blood, because both the The authors declare they have no conflict of interest. arterial and venous systems are not devoid of the vessel walls. The exchange is possible due to the fact References that the outer layers of veins and arteries connect 1. Hayward J, Baker M. A comparative study of the role of the cerebral blood in the regulation of brain temperature in five mammals. Brain Res. into the common tunica adventitia [23]. The inner 1969;16:417-40; DOI:10.1016/0006-8993(69)90236-4. muscular layer of arterioles is reduced to 3-5 layers 2. Caputa M. Mechanizmy obrony mózgu przed przegrzaniem u człowieka of muscle cells. Venous blood is separated from ar- i niektórych innych gatunków ssaków. Toruń: Roz UMK; 1982. 3. Strauss W, Hetem R, Mitchell D, Maloney S, O’Brien H, Meyer L, Fuller A. terial blood by five or six relatively thin vascular lay- Body water conservation through selective brain cooling by the carot- ers [6]. The mechanisms regulating the penetration id rete: a physiological feature for surviving climate change? Conserv. of neurotransmitters are not fully understood. The- Physiol. 2017; 5:1-15; DOI:10.1093/conphys/cow078. 4. Hetem RS, Strauss WM, Fick LG, Maloney SK, Meyer LCR, Fuller A, re are differences related to the oestrus cycle. The Shobrak M, Mitchell D. Selective brain cooling in Arabian oryx (Oryx countercurrent transfer of beta-endorphin takes leucoryx): a physiological mechanism for coping with aridity? JEB. place during the early luteal phase in the breeding 2012;215(22):3917-24; DOI:10.1242/jeb.074666. 5. Krzymowski T, Skipor J, Grzegorzewski W. Cavernous sinus and ca- season, but not during seasonal anoestrus. Studies rotid rete of sheep and sows as a possible place for countercurrent showed that the efficiency of the permeability of exchange of some neuropeptides and steroid hormones. Anim Rep Sci oxytocin [20] and LHRH in pigs [6, 24] depends on 1992;29;225-40. 6. Krzymowski T, Stefańczyk-Krzymowska S, Muszak J, Gilun P, Koziorows- the day of the oestrous cycle. Moreover, there may ki M. Cavernous sinus and its mysterious physiological functions: facts a link between the LH and oestradiol concentration and hypotheses Acta Biol Crac. 2014;55/56: 7–15. in blood [6]. Another role of the cavernous sinus 7. McKenna M, Bell S. Classification of mammals above the species level. New York: Columbia University Press; 1997. system in the rete mirabile is to transport the re- 8. Graczyk S, Zdun M. The structure of the rostral epidural rete mirabile in gulator of neurogenic carbon monoxide (CO). The selected representatives of the Cervidae and Bovidae families. Acta Zool. energy from visible light stimulates the production 2021;00, 1–6; DOI:10.1111/azo.12391. 9. Kiełtyka-Kurc A, Frąckowiak H, Nabzdyk M, Kowalczyk K, Zdun M, Tołk- of carbon monoxide by the retina, which penetrates acz M. The arteries on the base of the brain in the camelids. Ital J Zool. through the cavernous sinus into the vessels of the 2014;81:215–20; DOI:10.1080/11250003.2014.901428. rostral epidural rete mirabile, and causes changes 10. Al Aiyan A, Menon P, Al Darwich A, Almuhairi F, Alnuaimi S, Bulshawareb A, Qablan M, Shehab S. Descriptive analysis of cerebral arterial vascular in the activity of the brain [25]. Being a physiologi- architecture in dromedary camel (Camelus dromedarius). Front Neuro- cal regulator, carbon monoxide has decisive influen- anat. 2019;13:67; DOI:10.3389/fnana.2019.00067. ce on the brain function as the main biological clock. 11. Jerbi H, Khalid S, Perez W. Morphometric study of the rostral epi- dural rete mirabile in the dromedary (Camelus dromedarius Lin- It alters the expression of the Per and Cry genes, naeus 1758). Int J Morph. 2016;34(4):1429-35; DOI:10.4067/ which modulate the circadian rhythm and seasonal S0717-95022016000400042. cycles [26]. According to available scientific publi- 12. International Committee on Veterinary Gross Anatomical Nomencla- ture. Nomina anatomica veterinaria. 6th ed. Hannover: Editorial Com- cations, the rostral epidural rete mirabile in Cameli- mittee Germany (Hanover), Belgium (Ghent), U.S.A. (Columbia), Brazil formes is more strongly developed than in the other (Rio de Janeiro); 2017. suborders [8, 10]. This increases the contact surface 13. Simoens P, Lauwers H, De Geest J, De Schaepdrijver L. Functional mor- phology of the cranial retia mirabilia in the domestic mammals. Schweiz between the arterial and venous systems. It may be Arch Tierh. 1987;129:295-307. an adaptation to its function. However, physiologi- 14. Brudnicki W. Basilar arteries of the brain in domestic goat (Capra hir- cal tests are necessary to confirm this hypothesis. cus). EJPAU 2000;3:2. 15. Dieguez G, Conde V, Gomez B, Iglesias J, Marin J, Lluch S. Rete mirabile of goat: in vitro effects of adrenergic stimulation. Brain Res. 1983;289:281- Conclusions 4; DOI: 10.1016/0006-8993(83)90028-8. The rostral epidural rete mirabile, formed from 16. Dieguez G, García � A, Conde M, Gomez B, Santamaría � L, Lluch S. In vi- tro studies of the carotid rete mirabile of Artiodactyla. Microvasc Res. numerous anastomotic arteries, is a well-develo- 1987;33:143-54; DOI: 10.1016/0026-2862(87)90013-6. ped, even structure, with an elongated oval shape. 17. Dieguez G, García- � Villalón A, Gomez B, Lluch S. Hemodynamic signifi- Its rostral section is particularly well- developed. cance of the carotid rete during changes in arterial blood pressure. Am J Physiol. 1988;254:770-5; DOI:10.1152/ajpregu.1988.254.5.R770. The vessels of the rete are embedded in the caver- 18. O’Brein HD, Bourke J. Physical and computional fluid dynamics mod- nous sinus. The rostral segment is particularly well- els for the hemodynamics of the artiodactyl carotid rete. J Theor Biol. -developed due to the strong extensive rostral bran- 2015;386:122-31; DOI:10.1016/j.jtbi.2015.09.008. 19. Strauss AM, Hetem RS, Mitchell D, Maloney SK, Meyer LCR, Fuller A. ches to the rete. Selective Brain Cooling Reduces Water Turnover in Dehydrated Sheep. PLoS One. 2015;10(2):e0115514; DOI:10.1371/journal.pone.0115514. Ethical approval 20. Grzegorzewski W, Skipor J, Wąsowska B, Krzymowski T. Counter current The research related to animal use has been complied with all the transfer of oxytocin from the venous blood of the perihypophyseal cav- relevant national regulations and institutional policies for the care ernous sinus to the arterial blood of carotid rete supplying the hypoph- and use of animals. As the research material was collected posthu- ysis and brain depends on the phase of the estrous cycle in pigs. Biol mously, no Ethical Committee approval is needed for this study. Reprod. 1995;52:139-44; DOI:10.1095/biolreprod52.1.139. 21. Skipor J, Wąsowska B, Grzegorzewski W, Zezula-Szpyra A, Ste- fańczyk-Krzymowska S, Triery J. Transfer of dopamine by counter-cur- Acknowledgements rent mechanism in the ewes changes with endocrine stage. Biog Amin. Not applicable. 2001;16:431-45. 22. Skipor J, Wąsowska B, Picard S, Thiery J. Dopamine asses to the mediane Corresponding author eminence and brain throughout the vascular pathway in seep. Reprod Maciej Zdun DVM, PhD, Department of Basic and Preclinical Scien- Biol. 2004;4:91-106. ces, Institute of Veterinary Medicine, Nicolaus Copernicus Univer- 23. Khamas WA, Ghoshal NG, Bal HS. Histomorphologic structure of the sity in Toruń, Lwowska 1, 87-100 Toruń, +48 56 611 22 31, e-mail: carotid rete-cavernous sinus complex and its functional importance in maciejzdun@umk.pl. sheep (ovis aries). Am J Vet Res. 1984;45:156-8. 109 Zdun et al. Medical Journal of Cell Biology (2021) 24. Grzegorzewski W, Skipor J, Wąsowska B, Krzymowski T. Countercurrent transfer of 125I-LHRH in the perihypophyseal cavernous sinus-carot- id rete vascular complex, demonstrated on isolated pig heads perfused with autologous blood. Dom Ani Endoc. 1997;14:149-60; DOI:10.1016/ s0739-7240(97)00004-0. 25. Oren D. Humoral phototransduction: blood is messenger. Neuroscien- tist. 1996;2:207-10; DOI:10.1177/107385849600200408. 26. Gilun P, Stefańczyk-Krzymowska S, Romerowicz-Misielak M, Tabęc- ka-Lonczynska A, Przekop F, Koziorowski M. Carbon monoxide-mediat- ed humoral pathway for the transmission of light signal to the hypothal- amus. J Phys Pharm. 2013;64:761-72. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Advances in Cell Biology de Gruyter

The rostral epidural rete mirabile of the llama as a place of retrograde transport of various substances – anatomical basics

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Abstract

The aim of this study was to analyse the structure of the rostral epidural rete mirabile in the llama. Some specimens were prepared by injecting stained chemically cured acrylic into the bilateral common carot- id arteries. After about 1 month received vascular corrosion casts on the bone scaffold. Some specimens made using red and blue latex introduced into the bilateral common carotid arteries and the bilateral external jugular vein. The rostral epidural rete mirabile is a well-developed, bilateral structure composed of numerous arteries, which are multiply anastomosed with each other. The cranial section of the rete is asymmetrical. Its lateral part is much better developed, because there are rostral branches to the rostral epidural rete mirabile at this point. The arterial vessels are not accompanied by homonymous veins. How- ever, the arteries of the rostral epidural rete mirabile are accompanied by venous vessels of the cavernous sinus. That rete plays an important role in selective brain cooling, the conservation of body water, and ret- rograde transport of neurotransmitters. CO, GnRH, beta-endorphin, progesterone, testosterone, oxytocin, LHRH and dopamine diffuse from the venous blood of the cavernous sinus to the arterial blood of the ros- tral epidural rete mirabile. Running title: The rostral epidural rete mirabile of the llama Keywords: carbon monoxide, even-toed ungulates, neurotransmitters, RERM Department of Basic and Preclinical Sciences, Institute of Veterinary Medicine, Nicolaus Copernicus University in Toruń, Toruń, Poland *Correspondence: maciejzdun@umk.pl Full list of author information is available at the end of article 106 Zdun et al. Medical Journal of Cell Biology (2021) the blood vessels on the tissues of individual ani- Introduction mals. The names of the anatomical structures were The arterial system of the head of even-toed standardised according to the Nomina Anatomica ungulates is characterised by the presence of the Veterinaria [12]. rostral epidural rete mirabile. Due to the location of this rete in the cavernous sinus, it plays an im- portant role in selective brain cooling [1-3], the Results conservation of body water [4], and retrograde Blood reaches the rostral epidural rete mirabile transport of neurotransmitters [5, 6]. The Artiodac- (rete mirabile epidurale rostrale) through the pa- tyla order (even-toed ungulates) includes numero- ired common carotid artery (arteria carotis commu- us species of animals inhabiting almost all climatic nis) and the external carotid artery (arteria carotis zones of our planet, which can adapt to various externa), which is an extension of the former vessel. environmental conditions, e.g. animals of the Came- The internal carotid artery (arteria carotis interna) liformes, Ruminantia, and Suiformes suborders [7]. branches off in the place where the common carotid The construction of the rostral epidural rete mirabi- artery becomes the external carotid artery. le in selected representatives of ruminants has been The internal carotid artery passes through the well described [8]. Numerous authors describing jugular foramen and joins the rostral epidural rete the vessels of the encephalon base in Cameliformes mirabile. Moreover, this rete is composed of nume- mentioned the rete [9, 10], but did not describe it rous rostral branches to the rostral epidural rete in detail. There has been a description of the mor- mirabile (rami rostrales ad rete mirabile epidurale phometric characteristics of the rostral epidural rostrale) and the caudal branch to the rostral epi- rete mirabile of the dromedary – a representative of dural rete mirabile (ramus caudalis ad rete mirabi- the Old World camelids [11], but this structure has le epidurale rostrale). The rostral branches branch not been described in any representative of the New from the maxillary artery (arteria maxillaris) and World camelids. Each of the suborders of even-toed the external ophthalmic artery (arteria ophthalmi- ungulates differs in the structure of the rostral epi- ca externa). The caudal branch was very thin and it dural rete mirabile. was lacking from one specimen bilaterally and one As there have been numerous scientific publi- specimen unilaterally. cations on the functional nature of this vascular The rostral epidural rete mirabile is a well-develo- region in species of the Ruminantia and Suiformes ped, bilateral structure located on the corpus of the suborders, the aim of this study was to analyse the basisphenoid bone, on the lateral sides of the hypo- structure of the rostral epidural rete mirabile in physial fossa (Fig. 1). It is composed of numerous the llama – a representative of the Cameliformes arteries, which are multiply anastomosed with each suborder. This study may be useful for physiologi- other. The shape of the rostral epidural rete mirabile cal examinations of other suborders of even-toed resembles an elongated oval. The cranial section of ungulates. the rete is asymmetrical. Its lateral part is much bet- ter developed, because there are rostral branches to Material and methods the rostral epidural rete mirabile at this point. At the The study was conducted on 5 specimens of the half-length of the cross-section of the rostral epidu- llama of the Llama subfamily, Cameliformes subor- ral rete mirabile its shape is the most similar to an der. The research material was collected from priva- oval and the rete is composed of tiny vessels of simi- te breeders posthumously. lar diameters. The bilateral retes were connected by Three specimens were prepared by injecting numerous vessels in the caudal section. The number stained chemically cured acrylic DURACRYL PLUS of vessels in the rete ranged from 48 to 61. (SpofaDental, Jičí�n) into the bilateral common ca- The rostral cerebral artery (arteria cerebri rostra- rotid arteries. The specimens were cured after abo- lis) and the caudal communicating artery (arteria ut 20 min. Next, the material was enzymatically ma- communicans caudalis) emerge from the rete. These cerated with Persil powder (Henkel, Düsseldorf ) at vessels are the main arteries forming the cerebral 42°C for about 1 month. The procedure resulted in arterial circle (circulus arteriosus cerebri). vascular corrosion casts on the bone scaffold. Two The arterial vessels are not accompanied by specimens were prepared with another method. homonymous veins. However, the arteries of the Liquid LBS 3060 red latex was introduced into the rostral epidural rete mirabile are accompanied by bilateral common carotid arteries. Moreover, liquid venous vessels of the cavernous sinus (sinus caver- blue latex was introduced into the bilateral exter- nosus). The rostral epidural rete mirabile is embed- nal jugular vein. Next, the material was immersed ded in the cavernous sinus. There are numerous in a 5% formalin solution, where it hardened after small spaces, resulting in a spongy structure of this 7 days. Next surgical instruments were used to ma- sinus. These spaces are filled with vessels of the nually dissect the arteries and to obtain images of rostral epidural rete mirabile. 107 Zdun et al. Medical Journal of Cell Biology (2021) FIGURE 1 Corrosion cast of the rostral epidural rete mirabile 1- rostral epidural rete mirabile 1’ – rostral part of the rete mirabile with rostral branches to the rete 2 – internal carotid artery 3 – caudal branch to the rete mirabile Discussion Bourke [18] also concluded that the rostral epidural The internal carotid artery is one of the vessels rete mirabile was structurally incapable of reducing supplying blood to the rostral epidural rete mirabile the pressure of blood flowing to the brain. Regard- in Cameliformes. It has been described in the Bac- less of whether the rete regulates the flow of blood trian camel, dromedary, llama, and guanaco [9-11]. to the brain or not, many authors see its physiolo- The maxillary artery, which is a direct extension of gical role in the selective brain cooling mechanism. the external carotid artery, splits into the caudal This mechanism was described by Hayward and branch to the rostral epidural rete mirabile and the Backer in 1969 [1]. Its essence is to cool the warmer rostral branches to the rete. The rostral branches blood flowing through the arteries to the brain. The- to the rete branching from the maxillary artery and se arteries form a vast pool in numerous vessels of the external ophthalmic artery are the main vessels the rete washed by cooler blood returning from the supplying blood to the rete in Cameliformes [9-11]. nasal cavity and flowing through the cavernous si- Apart from that, there is a weak caudal branch to nus [1-3, 13]. As a result, during muscular effort the the rostral epidural rete mirabile, which Al Aiyan et animal can maintain the temperature of its brain at al. defined as the middle meningeal artery [10]. 40.5°C. Research conducted on Dorper sheep also A cross-section of the rostral epidural rete mi- proved the importance of selective brain cooling for rabile revealed a bundle of tiny vessels of similar the conservation of body water [19]. diameter. According to Simoens et al. [13], the rete Apart from that, the rostral epidural rete mirabi- has a bipolar structure. Researchers have been in- le together with the cavernous sinus are responsi- terested in the function of this rete for a long time. ble for the retrograde transport of neurotransmit- According to some authors, the rostral epidural rete ters, which is a lesser-known fact. Studies on pigs mirabile regulates the blood flow [14]. However, and sheep have shown that there is GnRH, beta-en- Dieguez et al. [15-17] observed that the arteries dorphin, progesterone or testosterone [5], oxytocin forming the rete did not respond to adrenergic sti- [20], and dopamine [21, 22] diffusion from the veno- mulation and concluded that they did not actively us blood of the cavernous sinus to the arterial blood regulate the flow of blood to the brain. O’Brien and of the rostral epidural rete mirabile. Arterial blood 108 Zdun et al. Medical Journal of Cell Biology (2021) Conflict of interest statement is not mixed with venous blood, because both the The authors declare they have no conflict of interest. arterial and venous systems are not devoid of the vessel walls. The exchange is possible due to the fact References that the outer layers of veins and arteries connect 1. Hayward J, Baker M. A comparative study of the role of the cerebral blood in the regulation of brain temperature in five mammals. Brain Res. into the common tunica adventitia [23]. The inner 1969;16:417-40; DOI:10.1016/0006-8993(69)90236-4. muscular layer of arterioles is reduced to 3-5 layers 2. Caputa M. Mechanizmy obrony mózgu przed przegrzaniem u człowieka of muscle cells. Venous blood is separated from ar- i niektórych innych gatunków ssaków. Toruń: Roz UMK; 1982. 3. Strauss W, Hetem R, Mitchell D, Maloney S, O’Brien H, Meyer L, Fuller A. terial blood by five or six relatively thin vascular lay- Body water conservation through selective brain cooling by the carot- ers [6]. The mechanisms regulating the penetration id rete: a physiological feature for surviving climate change? Conserv. of neurotransmitters are not fully understood. The- Physiol. 2017; 5:1-15; DOI:10.1093/conphys/cow078. 4. Hetem RS, Strauss WM, Fick LG, Maloney SK, Meyer LCR, Fuller A, re are differences related to the oestrus cycle. The Shobrak M, Mitchell D. Selective brain cooling in Arabian oryx (Oryx countercurrent transfer of beta-endorphin takes leucoryx): a physiological mechanism for coping with aridity? JEB. place during the early luteal phase in the breeding 2012;215(22):3917-24; DOI:10.1242/jeb.074666. 5. Krzymowski T, Skipor J, Grzegorzewski W. Cavernous sinus and ca- season, but not during seasonal anoestrus. Studies rotid rete of sheep and sows as a possible place for countercurrent showed that the efficiency of the permeability of exchange of some neuropeptides and steroid hormones. Anim Rep Sci oxytocin [20] and LHRH in pigs [6, 24] depends on 1992;29;225-40. 6. Krzymowski T, Stefańczyk-Krzymowska S, Muszak J, Gilun P, Koziorows- the day of the oestrous cycle. Moreover, there may ki M. Cavernous sinus and its mysterious physiological functions: facts a link between the LH and oestradiol concentration and hypotheses Acta Biol Crac. 2014;55/56: 7–15. in blood [6]. Another role of the cavernous sinus 7. McKenna M, Bell S. Classification of mammals above the species level. New York: Columbia University Press; 1997. system in the rete mirabile is to transport the re- 8. Graczyk S, Zdun M. The structure of the rostral epidural rete mirabile in gulator of neurogenic carbon monoxide (CO). The selected representatives of the Cervidae and Bovidae families. Acta Zool. energy from visible light stimulates the production 2021;00, 1–6; DOI:10.1111/azo.12391. 9. Kiełtyka-Kurc A, Frąckowiak H, Nabzdyk M, Kowalczyk K, Zdun M, Tołk- of carbon monoxide by the retina, which penetrates acz M. The arteries on the base of the brain in the camelids. Ital J Zool. through the cavernous sinus into the vessels of the 2014;81:215–20; DOI:10.1080/11250003.2014.901428. rostral epidural rete mirabile, and causes changes 10. Al Aiyan A, Menon P, Al Darwich A, Almuhairi F, Alnuaimi S, Bulshawareb A, Qablan M, Shehab S. Descriptive analysis of cerebral arterial vascular in the activity of the brain [25]. Being a physiologi- architecture in dromedary camel (Camelus dromedarius). Front Neuro- cal regulator, carbon monoxide has decisive influen- anat. 2019;13:67; DOI:10.3389/fnana.2019.00067. ce on the brain function as the main biological clock. 11. Jerbi H, Khalid S, Perez W. Morphometric study of the rostral epi- dural rete mirabile in the dromedary (Camelus dromedarius Lin- It alters the expression of the Per and Cry genes, naeus 1758). Int J Morph. 2016;34(4):1429-35; DOI:10.4067/ which modulate the circadian rhythm and seasonal S0717-95022016000400042. cycles [26]. According to available scientific publi- 12. International Committee on Veterinary Gross Anatomical Nomencla- ture. Nomina anatomica veterinaria. 6th ed. Hannover: Editorial Com- cations, the rostral epidural rete mirabile in Cameli- mittee Germany (Hanover), Belgium (Ghent), U.S.A. (Columbia), Brazil formes is more strongly developed than in the other (Rio de Janeiro); 2017. suborders [8, 10]. This increases the contact surface 13. Simoens P, Lauwers H, De Geest J, De Schaepdrijver L. Functional mor- phology of the cranial retia mirabilia in the domestic mammals. Schweiz between the arterial and venous systems. It may be Arch Tierh. 1987;129:295-307. an adaptation to its function. However, physiologi- 14. Brudnicki W. Basilar arteries of the brain in domestic goat (Capra hir- cal tests are necessary to confirm this hypothesis. cus). EJPAU 2000;3:2. 15. Dieguez G, Conde V, Gomez B, Iglesias J, Marin J, Lluch S. Rete mirabile of goat: in vitro effects of adrenergic stimulation. Brain Res. 1983;289:281- Conclusions 4; DOI: 10.1016/0006-8993(83)90028-8. The rostral epidural rete mirabile, formed from 16. Dieguez G, García � A, Conde M, Gomez B, Santamaría � L, Lluch S. In vi- tro studies of the carotid rete mirabile of Artiodactyla. Microvasc Res. numerous anastomotic arteries, is a well-develo- 1987;33:143-54; DOI: 10.1016/0026-2862(87)90013-6. ped, even structure, with an elongated oval shape. 17. Dieguez G, García- � Villalón A, Gomez B, Lluch S. Hemodynamic signifi- Its rostral section is particularly well- developed. cance of the carotid rete during changes in arterial blood pressure. Am J Physiol. 1988;254:770-5; DOI:10.1152/ajpregu.1988.254.5.R770. The vessels of the rete are embedded in the caver- 18. O’Brein HD, Bourke J. Physical and computional fluid dynamics mod- nous sinus. The rostral segment is particularly well- els for the hemodynamics of the artiodactyl carotid rete. J Theor Biol. -developed due to the strong extensive rostral bran- 2015;386:122-31; DOI:10.1016/j.jtbi.2015.09.008. 19. Strauss AM, Hetem RS, Mitchell D, Maloney SK, Meyer LCR, Fuller A. ches to the rete. Selective Brain Cooling Reduces Water Turnover in Dehydrated Sheep. PLoS One. 2015;10(2):e0115514; DOI:10.1371/journal.pone.0115514. Ethical approval 20. Grzegorzewski W, Skipor J, Wąsowska B, Krzymowski T. Counter current The research related to animal use has been complied with all the transfer of oxytocin from the venous blood of the perihypophyseal cav- relevant national regulations and institutional policies for the care ernous sinus to the arterial blood of carotid rete supplying the hypoph- and use of animals. As the research material was collected posthu- ysis and brain depends on the phase of the estrous cycle in pigs. Biol mously, no Ethical Committee approval is needed for this study. Reprod. 1995;52:139-44; DOI:10.1095/biolreprod52.1.139. 21. Skipor J, Wąsowska B, Grzegorzewski W, Zezula-Szpyra A, Ste- fańczyk-Krzymowska S, Triery J. Transfer of dopamine by counter-cur- Acknowledgements rent mechanism in the ewes changes with endocrine stage. Biog Amin. Not applicable. 2001;16:431-45. 22. Skipor J, Wąsowska B, Picard S, Thiery J. Dopamine asses to the mediane Corresponding author eminence and brain throughout the vascular pathway in seep. Reprod Maciej Zdun DVM, PhD, Department of Basic and Preclinical Scien- Biol. 2004;4:91-106. ces, Institute of Veterinary Medicine, Nicolaus Copernicus Univer- 23. Khamas WA, Ghoshal NG, Bal HS. Histomorphologic structure of the sity in Toruń, Lwowska 1, 87-100 Toruń, +48 56 611 22 31, e-mail: carotid rete-cavernous sinus complex and its functional importance in maciejzdun@umk.pl. sheep (ovis aries). Am J Vet Res. 1984;45:156-8. 109 Zdun et al. Medical Journal of Cell Biology (2021) 24. Grzegorzewski W, Skipor J, Wąsowska B, Krzymowski T. Countercurrent transfer of 125I-LHRH in the perihypophyseal cavernous sinus-carot- id rete vascular complex, demonstrated on isolated pig heads perfused with autologous blood. Dom Ani Endoc. 1997;14:149-60; DOI:10.1016/ s0739-7240(97)00004-0. 25. Oren D. Humoral phototransduction: blood is messenger. Neuroscien- tist. 1996;2:207-10; DOI:10.1177/107385849600200408. 26. Gilun P, Stefańczyk-Krzymowska S, Romerowicz-Misielak M, Tabęc- ka-Lonczynska A, Przekop F, Koziorowski M. Carbon monoxide-mediat- ed humoral pathway for the transmission of light signal to the hypothal- amus. J Phys Pharm. 2013;64:761-72.

Journal

Advances in Cell Biology – de Gruyter

Published: Sep 1, 2021

Keywords: carbon monoxide; even-toed ungulates; neurotransmitters; RERM

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