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Comparative and functional anatomy of cerebrally related retial systems in the family Monodontidae (order Cetacea) Vogl, Adalbert Wayne

Abstract

In this study, I consider the comparative and functional anatomy of cerebrally related retial systems in the two constituent species (Monodon monoceros and Delphinapterus leucas) of the family Monodontidae (order Cetacea). The internal carotid arteries, the "classical" vessels of cerebral supply in vertebrates, are completely non-functional as cerebral supply vessels in the Monodontidae. Moreover, there are no other channels that contribute directly to intracranial supply. Rather, the brain, or more precisely, the entire central nervous system, is vascularized indirectly via an extensive arterial plexus or rete mirabile. This plexus is found in the thorax, lumbar region, neural canal and cranium. Vessels that contribute to retial formation are numerous and include those which in other mammals contribute directly to supply of the central nervous system and/or its membranes. Efferent retial vessels are few and include two pairs of subdural intracranial trunks that supply the brain, and numerous small segmental vessels that penetrate the spinal dura and vascularize the spinal cord. Subdural arterial circulation in the Monodontidae is modified after the basic mammalian pattern. Within the cranium, it is characterized by: (1) an incomplete circle of Willis (due to (a) independence of the anterior cerebral arteries and (b) the lack of anastomoses between the two pairs of trunks which take origin from the rete), (2) extensive cortical supply by the anterior choroid arteries, and (3) absence of a vertebral basilar system. Subdural arteries coursing to the spinal cord do so mainly between successive ventral spinal roots. An A. radicularis magna is not evident, nor are anterior or posterior spinal arteries. Hence, there are differences between the subdural circulatory patterns in the Monodontidae and those in other mammals, however the major site of vascular modification is epidural with formation of the rete mirabile. Though gross retial anatomy is the same in Monodon monoceros and Delphinapterus leucas, and is generally similar to that described for other odontocetes, there are two related characteristics that appear species specific: thoracic retial size and the number of intercostal spaces supplied by the supreme intercostal arteries. Both are larger in Monodon monoceros, as are hematological values (hematocrit and hemoglobin concentration) which, in this study, are used as indices of diving ability. These data are consistent with the hypothesis that cerebral related retia in the Cetacea are related to the diving habit. Microscopically, the rete generally consists of small muscular arteries embedded in fatty connective tissue interlaced with a few nerve trunks and veins. Arterial walls are characterized by a distinct internal elastic lamella, a tunica media of 12-14 layers of vascular smooth muscle, and an adventitia of alternating layers of collagen and elastin. Retial arteries are at best poorly innervated. The substructure of retial arteries resembles that of other mammalian arteries except for the presence of large deposits of glycogen (alpha particles) in vascular smooth muscle and endothelial cells. On the basis of this observation, and theoretical considerations, I generate the hypothesis that the rete may contribute to blood glucose levels during a dive. This hypothesis could not be tested directly, hence I chose an indirect approach involving biochemical and ultrastructural analyses. I conclude that free glucose release is not a major function of the rete since: (1) G-6-phosphatase activities are low, (2) LDH electrophoretic profiles suggest that most stored glycogen is used intrinsically, and (3) I could not demonstate glycogen deposits in retial vessels of other species. All proposed retial functions are evaluated, and I conclude that the system probably functions in a mechanical way (pressure reservoir) and that it does so passively.

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