Lametschwandtner A and Minnich B (2018), Microvascular anatomy of the brain of the adult...

XB-ART-54842

J Morphol 2018 Jul 01;2797:950-969. doi: 10.1002/jmor.20824.

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Microvascular anatomy of the brain of the adult pipid frog, Xenopus laevis (Daudin): A scanning electron microscopic study of vascular corrosion casts.

Lametschwandtner A , Minnich B .

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To demonstrate the 3D microvascular anatomy of the brain of the model organism Xenopus laevis Daudin scanning electron microscopy of vascular corrosion casts was correlated with light microscopy of stained 7 µm thick serial tissues sections. Results showed that supplying arteries descended from the leptomeningeal surface without remarkable branchings straight to the subventricular zone where they branched and capillarized. Capillaries showed few H- and/or Y-shaped anastomoses during their centrifugal course toward the leptomeningeal surface where they drained into cerebral venules and veins. Apart from the accessory olfactory bulb and the vestibule-cochlear nucleus where capillaries were densely packed, capillaries formed a wide-meshed 3D network throughout the brain parenchyma and thus contrasted to urodelian brains where hairpin-shaped capillaries descend from the leptomeningeal vessels into varying depths of the brain parenchyma. In about two-third of specimens, a closed arterial circle of Willis was found at the base of the brain. If this circle in Xenopus might serve the same two functions as in men is briefly discussed. Choroid plexuses of third and fourth ventricle were found to have a high venous, but a low arterial inflow via one small choroidal artery only. Findings are compared with previous studies on the vascularization of the anuran brain and discrepancies in respect to presence or absence of particular arteries and/or veins in Ranids, Bufonids, and Pipids studied so far are discussed with particular emphasis on the techniques used in the various studies published so far.

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Species referenced: Xenopus laevis
Genes referenced: tecta.2

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	Figure 1. Microvascular anatomy of the brain in adult X. laevis. Vascular corrosion cast. SEM. Ventral view displaying telencephalic hemispheres (tel), preoptic area (pa), hypothalamus (hyp), hypophysis (hy), and mesencephalic and rhombencephalic tegmentum (teg). Arterial vessels are red, venous vessels are blue, and meningeal vessels are green. Asterisks mark extravasates. For further abbreviations in this and following figures see the list of abbreviations
	Figure 2. Gross arterial supply and venous drainage of olfactory bulb (ob), telencephalon (tel), and preoptic area (pa). Ventral view
	Figure 3. Anatomy of the vertebro‐basilar arterial system. Inset a. Communicating arteries (arrows) bifurcate before they join the basilar artery (ba) bilaterally. Inset b. Asymmetric junctions of left (1) and right (2) communicating arteries with the basilar artery (3). Asterisks mark conductive bridges
	Figure 4. Microvascular anatomy of the ventral hypothalamo‐hypophysial region. Ventral aspect. Note the superficial infundibular artery (sia) which gives off a medially directed branch (large arrows) supplying the delicate capillary network of the retrochiasmatic (rostral) and infundibular (caudal) region. The parent artery bends toward caudal to supply the median eminence (me) via a medially directed branch (arrowheads) and the intermediate lobe of the hypophysis (ilhy) via a laterally directed terminal branch (small arrows)
	Figure 5. Same as Figure 4 but after removal of vascular beds of infundibular region (ventral hypothalamus) and hypophysis. Note the deeply penetrating branches of the superficial infundibular arteries (sia; arrowheads), the retroinfundibular communicating artery (rica) and the origin of prominent ascending rostral tegmental arteries (rta). Inset a. Histomorphology of (right) optic tectum (ot) and tegmentum (teg) of the mesencephalon. Paraplast embedded Goldner stained tissue section (7 µm). Transverse section at the level of the ascending rostral tegmental arteries (arrowheads). Arrow marks the mesencephalic ventricle. ir, infundibular recess. Inset b. Same as inset a, but slightly more caudal section. Note the horizontally running caudal branch of the (right) rostral tegmental artery (arrow) and its ascending branch (arrowhead)
	Figure 6. Arterial supply and venous drainage of the dorsal hypothalamus. Note the arterial supply via the deep infundibular artery (dia) and subependymally located rostral branches of rostral tegmental arteries (rta). The diencephalic vein (dv) drains rostral areas while the hypothalamic vein (hv) drains caudal areas
	Figure 7. Same specimen as in Figure 6, but after exposure of the deep infundibular artery by removal of overlaying vessels. Note that the artery runs without branching straight toward the subependymal zone where it branches into rostrally and caudally directed branches
	Figure 8. Internal microvascular anatomy of the brain of adult X. laevis. Sagittally sectioned vascular corrosion cast. Right half of the brain displaying telencephalon (tel), diencephalon (di) (without hypothalamus and hypophysis), mesencephalon (mes), cerebellum (cer), and rhombencephalon (rho). Asterisks mark conductive bridges
	Figure 9. Histomorphology of the brain of adult X. laevis. Paraplast embedding. Goldner stained sagittal section (7 µm) at a similar level as displayed in Figure 8. (1) anterior lobe of hypophysis, (2) intermediate lobe of hypophysis, (3) posterior lobe of hypophysis, (4) retroinfundibular communicating artery, and (5) encephalo‐posthypophysial portal vein
	Figure 10. Origin of the preoptic artery (poa) from the anterior branch of the cerebral carotid artery (ab). Note the coiling of the artery (arrowhead) and the side‐branch of the artery (arrow)
	Figure 11. Branching pattern of the preoptic artery (poa) within the subependymal zone of the preoptic area. Note the branches directed anteriorly, laterally, and caudally. Anterior is to the left
	Figure 12. Exposed terminal branching of the striatal artery (sa). Lateral view
	Figure 13. Microvascular anatomy of pallial, septal, and striatal areas. Transverse section. Oblique frontal view. Arrows mark external border between pallium and subpallium
	Figure 14. Course and subependymal branching of the striatal artery (sa). Fronto‐lateral view
	Figure 15. Origin, course, and areas of supply of the posterior telencephalic artery (pta). Inset a. Terminal portion of the posterior telencephalic artery (arrow). Inset b. Histomorphology of the right telencephalic hemisphere. Transverse section (7 µm). Goldner staining. Note the ascending posterior telencephalic artery (arrowheads)
	Figure 16. Obliquely ascending posterior telencephalic artery (pta) giving off a rostrally directed branch at the level of the dorsomedial pallium (arrowhead). The main trunk bends toward caudal and issues several branches (arrows). Inset a. Characteristic endothelial cell nuclei imprints (arrowheads) at the surface of a cast artery (posterior telencephalic artery). Imprints are longish and orientate parallel to the vessel axis. Inset b. Characteristic endothelial cell nuclei imprints (arrowheads) at the surface of a cast vein (interhemispheric vein). Imprints are oval to roundish and orientate randomly
	Figure 17. Bifurcation of the posterior telencephalic artery (pta) at the border area between medio‐caudal poles of telencephalic hemispheres (tel) and choroid plexus of the third ventricle (cp III)
	Figure 18. Microvascular anatomy of the pial surface of the posterior pole of the telencephalon (tel), epithalamus (epi), thalamus (th), optic tectum (ot), mesencephalic, and rhombencephalic tegmentum (teg). Lateral view. Rostral is to the right. Note the small caliber of the diencephalic artery (da) which shares a common stem with a lateral tegmental artery (arrow). The posterior superior mesencephalic artery (psma) shares a common stem with the inferior mesencephalic (tegmental) artery (arrowhead)
	Figure 19. Microvascular anatomy of caudal dorsal (dp) and lateral pallium (lp), epithalamus (epi) and optic tectum (ot). Dorso‐lateral view. Note the prominent oblique cranial vein (ocv) and the medially located longitudinal mesencephalic vein (lmv) which by two tributaries (arrows) drains epithalamic, thalamic and rostral, and lateral areas of the optic tecta
	Figure 20. Branch of the diencephalic artery (da) within the (right) dorsal thalamus (dth) after removal of subependymal vessels. Ventricular view. Rostral is to the left
	Figure 21. Microvascular anatomy of the brain of adult X. laevis. Dorsal view. Note the dorsal location of cranial veins
	Figure 22. Vascular patterns of paraphysis (par) and choroid plexus of the third ventricle (cp III). Dorsal aspect. Note the veins (v) draining medial pallial areas into the choroid plexus. Arrows indicate proposed direction of blood flow
	Figure 23. Isolated choroid plexus of the third ventricle. Same specimen as in Figure 22, but ventro‐lateral aspect. The interhemispheric vein (asterisk) continues as wide sinusoid within the plexus. Note the many sites of ongoing intussusceptive microvascular growth (arrows)
	Figure 24. Arterial supply and venous drainage of the mesencephalon (parts of the rostral optic tecta are removed). Anterior is at bottom. Note the prominent anterior inferior mesencephalic arteries (aima) which first penetrate deeply into subependymal areas and then curve in a semicircular manner (arrows). Branches from the posterior superior mesencephalic arteries (psma) radiate from caudally deep into the optic tecta (arrowheads)
	Figure 25. Origin and course of anterior superior mesencephalic artery (asma). Note the coiling of the artery at the rostrolateral area of the optic tectum (ot). Rostral is to the left
	Figure 26. Arterial supply and venous drainage of the left optic tectum. Rostral is to the left. Note the transverse course of the posterior superior mesencephalic artery (psma; arrowheads) within the cleft between optic tectum (ot) and cerebellum (hidden by the overlying choroid plexus of the fourth ventricle (cp IV)
	Figure 27. Arterial supply and venous drainage of the semicircular torus (st). Note the location of the innermost arteriole (arrowheads) close beneath the subependymal capillary bed and the radial arrangement of tectal vessels
	Figure 28. Origin of the rostral tegmental arteries (rta) from the retroinfundibular communicating artery (rica). Lateral view. Note the bifurcations of the arteries into anteriorly (small arrows) and posteriorly directed branches (large arrows)
	Figure 29. Course and branching pattern of branches of rostral tegmental arteries (rta). Note that caudal branches terminate in the lateral optic tectum (lot) and rostral branches in the rostral optic tectum (rot)
	Figure 30. Microvascular anatomy of the cerebellar (cer)—rhombencephalic (rho) area. Dorsal view. Choroid plexus of the fourth ventricle is removed to expose the rhombencephalic fossa (rf). Note the circumferentially running tegmental veins (arrowheads) which drain into the choroid plexus of the fourth ventricle. Asterisks mark conductive bridges
	Figure 31. Arterial supply and venous drainage of the cerebellum. Rostral is at top. Choroid plexus IV is removed to expose the course of the posterior superior mesencephalic artery (psma) within the cleft between cerebellum (cer) and optic tecta (ot). Note several small cerebellar arteries (arrowheads) branching off the posterior superior mesencephalic artery
	Figure 32. Vascular architecture of the rhombencephalic tegmentum (teg) and cochlear‐vestibular nuclear regions (cvr). Slightly parasaggitally sectioned rhombencephalon. Rostral is to the right. Note origin, course and branching patterns of central arteries (ca). Inset a. Central arteries (arrowheads) branching off the lateral circumference of the basilar artery (ba). Inset b. Central arteries branching immediately after their origin from the basilar artery (arrowheads)
	Figure 33. Branching patterns of central arteries. Dorsal view at bifurcating central arteries (ca) after removal of subependymal vessels. Note branches to right or left tegmental areas (arrowheads)
	Figure 34. Microvascular anatomy of the caudal rhombencephalon. Transverse section at the level indicated by the dashed line in Figure 30. Frontal view indicated by arrows in Figure 30. Note an ascending central artery (ca) supplying the right side and horizontally running branches of a more anterior central artery on the left side of the rhombencephalon
	Figure 35. Radial arrangement of rhombencephalic tegmental capillaries (c). Detail from Figure 34 (box). Specimen slightly tilted. Note H‐shaped (arrowhead) and Y‐shaped (arrows) branchings
	Figure 36. Gross arterial supply and venous drainage of olfactory bulb (ob), telencephalon (tel) and diencephalon (di). Ventro‐lateral view. Rostral is to the right. Note the lateral telencephalic vein (ltv) and its dorsal and ventral tributaries. Inset a. Confluence of cerebral veins at the level of the prootic foramen. Lateral view
	Figure 37. Course and caliber of the (right) oblique cranial vein (ocv). Lateral view at the optic tectum (ot), diencephalon (di), and caudal telencephalon (tel). Rostral is to the right
	Figure 38. Anatomy of the encephalo‐posthypophysial portal system. Ventral aspect. Hypophysis and caudal infundibulum are removed. Note the hypothalamic branch (hb) and the ventral tegmental branches (vtb) of the portal system
	Figure 39. Vascular anatomy of the hypophysis. Longitudinal section through mesencephalic tegmentum and hypophysis. Note the drainage of the encephalo‐posthypophysial portal system into the rostro‐dorsal area of the posterior lobe of the hypophysis (plhy)
	Figure 40. Venous drainage of the semicircular torus (st) into the anterior region of the choroid plexus of the fourth ventricle (cp IV). Medial aspect. Rostral is to the right
	Figure 41. Vascular anatomy of the roof (tela choroidea) of the fourth ventricle. Dorsal aspect. Note that the choroid plexus (cp IV) does not cover the entire length of the rhombencephalic fossa (rf)
	Figure 42. Arterial supply of the choroid plexus of the fourth ventricle by a small choroidal artery (cha). Note choroidal veins (cv) draining into the oblique occipital veins (oov)
	Figure 43. Major arteries and veins at the ventral surface of the brain of adult X. laevis. Ventral hypothalamus, hypophysis, and proximal portions of anterior and posterior branches of the cerebral carotid arteries are removed. Note the origin of the circumferential tegmental veins (arrowheads) at the ventral midline (arrows)
	Figure 44. Vascular anatomy of the choroid plexus of the fourth ventricle. Ventral aspect. Note marginal choroidal tela (cht), central choroidal folds (cf), and left oblique occipital vein (oov). Arrowheads point at the sites where rhombencephalic tegmental veins drain into the choroid plexus
	Figure 45. Detail from Figure 44. Vertical, transversely orientated choroidal folds (cf) made up from a dense 2D network of sinusoids. Choroidal folds reveal ventral venules (vv) which interconnect at the midline. Note the many sites of ongoing intussusceptive angiogenesis (arrows)
	Figure 46. Microvascular anatomy of the accessory olfactory bulb (aob). Ventro‐lateral view. Note the dense capillary bed supplied by a branch of the lateral olfactory artery (loa) and the drainage by ventral, lateral, and dorsal branches of the lateral telencephalic vein (ltv)
	Figure 47. Microvascular pattern of the cochlear‐vestibular complex as seen from the rhombencephalic fossa. By the parasagittal section part of the subependymal capillary bed is sectioned‐off and underlying supplying arterioles are seen. Note that several capillaries join into single venules which ascend parallel to drain into the choroid plexus of the fourth ventricle (cp IV)

References [+] :

Abbie, The Morphology of the Fore-Brain Arteries, with Especial Reference to the Evolution of the Basal Ganglia. 1934, Pubmed