Yak and Tibetan sheep are the native domestic animals adapted to higher altitude plateau areas, and have showed excellent productivity in harshly cold, low-pressure and low-oxygen environments. The cerebral arterial system supplies nutrients and oxygen to the brain tissue. In order to study the morphological structures and anatomical characteristics of the constituent arteries of the cerebral arterial system in yak and Tibetan sheep, and explore mechanisms of environmental adaptation related to cerebral blood flow and its regulation, this work investigated morphological features, gross anatomic structures, arterial diameters and the superstructure of the cerebral arterioles in yak and Tibetan sheep, and compared differences with those of the low-altitude cattle and sheep vascular corrosion casts and the comparative anatomical methodology.
Results were as follows:
1. Vascular corrosion casts of the cerebral arterial system from the plateau yak was obtained for the first time in this research. The cerebral arterial system of the yak and cattle were divided into three parts: the intracranial cerebral arteries, epidural retia mirabile and extracranial supply arteries. By comparison of the basic structure, vessel formation and arterial diameters of the cerebral arterial system between the two species, we found that the gross morphological features, main arterial formation and arterial diameters were similar. In some anatomical properties, however, yak showed unique morphological structures.
2. In the intracranial cerebral arteries of the two species, the anterior-posterior diameter of the cerebral arterial circle in the yak was shorter than that of cattle (21.44 mm vs. 30.33 mm), the left-right diameter of the posterior circle was wider (20.48 mm vs. 18.98 mm) and vessels of the circle were curver than that of cattle, and distance between the cerebral carotid arteries was less (9.32 mm vs. 12.07mm) than that of cattle. Arterial diameters measurements showed that the internal diameters of the main cerebral arteries of yak were thinner than those of cattle but with no significant differences (P>0.05). The diameters of the middle cerebra artery and posterior communicating artery of yak were significantly thinner than those of cattle (P<0.05). In the structure of the extracranial supply arteries, vessel spread and arterial diameters were very similar between the yak and cattle. The decreasing ratio of the main extracranial arterial diameters in the yak were milder than that of cattle, and the distribution ratios of blood flow from the maxillary artery entering the anterior epidural retia mirabile was higher than those of cattle (33.12% vs. 30.42% ).
3. Main structure of the epidural retia mirabile of the yak and cattle were divided into four parts: anterior epidural retia mirabile, posterior epidural retia mirabile, basi-occipital arterial plexus and anterior V-shaped extension. Analysis demonstrated that the morphological features and structural formation of the epidural retia mirabile of yak and cattle showed significant differences. Firstly, the anterior epidural retia mirabile of the yak was wider (33.98 mm vs. 30.23mm) and larger and showed a more developed posterior joint sections than those of cattle. Secondly, the anastomotic branches of the anterior epidural retia mirabile in the yak were significantly more abundant (6.73 vs. 5.22); thirdly, the communicating rami of the posterior epidural retia mirabile were significantly more abundant (5.43 vs. 3.21). The epidural retia mirabile of the yak received blood mainly from five arteries: the maxillary, occipital, vertebral, external ophthalmic and condylar arteries, similarto arterial sources of cattle.
4. Superstructure of the cerebral arterioles between the yak and cattle showed some differences. At arteriole diameters below 100μm, the vascular endothelium of cerebral arterioles in the yak was annular smooth muscle, and it is implied that the structure can increase blood flow resistance and may have a role in auto-regulating blood pressure. At diameters between 100μm and 300μm,the smooth muscle fibers of the yak cerebral arterioles were more slender and the imprints of the endothelial cell nuclei were more prominent than those of cattle.
5. We concluded that the unique anatomical structure of the cerebral arterial circle results in slows blood flow velocity, thereby supplying more nutrients and oxygen to the brain, and relatively developed intracranial arterial vessels in yak were beneficial to supplying more blood to the brain. The developed epidural retia mirabile of yak appears to play a vital role in buffering and regulating cerebral blood flow so as to meet the demand for nutrients and oxygen of the yak’s brain in the high-altitude plateau areas. In addition, superstructure of the cerebral arterioles in yak implied that the blood flow resistance was lesser and velocity was greater so as to supply more blood to the brain.
6. In contrast, we found that comparison of the gross anatomical features of the cerebral arterial system between Tibetan sheep and low-land sheep showed only minor differences such as individual cerebral arterial diameters, vessels spread, epidural retia mirabile size and superstructure of the cerebral arterioles. The epidural retia mirabile in the Tibetan sheep was longer than that of low-land sheep (22.99 mm vs. 20.96 mm, P<0.05). The diameters of the posterior communicating artery (1.36 mm) and maxillary artery (2.85 mm) were greater than those of low-land sheep (1.10 mm vs. 2.18 mm, P<0.05). In addition, in contrast to low-land sheep, the Tibetan sheep showed more developed cerebral arteria branches, more arterial spread and more abundant small branches.
7. The cross section of main cerebral arteries per unit weight of brain tissue in Tibetan sheep was slightly larger than those of low-land sheep (0.020 vs. 0.018), and the ratio of the cross section of main cerebral arteries and average body weight in the Tibetan sheep was higher than those of low-land sheep (0.050 vs. 0.043). Generally, we considered that there were more developed intracranial cerebral arteries in the Tibetan sheep, and it can be deduced that the blood volume serving the brain tissue was more abundant which might explain the superior adaptation to high altitudes of Tibetan sheep.
8. The superstructure of the cerebral arterioles in the Tibetan sheep showed prominent “oval” or “footprint” endothelial cell nuclei imprints and their edges were distinct at the diameters range about 60~160μm. The superstructure of the cerebral arterioles in low-land sheep showed mainly “spindle” endothelial cell nuclei imprints and imprints were not distinct. The superstructure of the cerebral arterioles in the Tibetan sheep showed relatively thicker smooth muscle fiber imprints and gap imprints at the diameters range about 200~300μm than those of low-land sheep. There were longer epidural retia mirabile, thicker cerebral arteries and more developed intracranial cerebral arterial branches in the Tibetan sheep, indicating that the cerebral arterial system in Tibetan sheep was more developed than that of low-land sheep. In addition, the Tibetan sheep showed prominent endothelial cell nuclei imprints in the cerebral arterioles and thick smooth muscle fiber. We deduced that Tibetan sheep may have stronger vessel contraction than low-land sheep. Consequently, these anatomical characteristics in Tibetan sheep appear to allow supply of blood more efficiently to the brain tissue via the cerebral arterial system and enhance regulation of cerebral arterial pressure. So we hypothesized that these might be morphological mechanisms of the Tibetan sheep allowing adaptation to plateau environments.