The carotid labyrinth in the primitive New Zealand frog, Leiopelma hochstetteri
The amphibian carotid labyrinth was first described in 1738, but its purpose has never been satisfactorily explained. Much of the extant literature has either been restricted to a particular aspect of the organ, or has been based on erroneous information. This thesis used the New Zealand frog Leiopelma hochstetteri because its primitive status might render some characteristics of the carotid labyrinth more clearly evident.
The "gross" anatomy of the tiny (0.5 mm diameter) organ was examined by wax-plate reconstruction and by scanning electron microscopy. The cytology of the capillary plexus tissue was studied by light and transmission electron microscopy using conventionally prepared sections. The higher resolution of the electron microscope permitted a more exact study of the innervation of the organ. Neurophysiological experiments were undertaken, but the very short (0.6 mm) and fine carotid nerve proved intractable. A study of the in vivo flow of blood through the labyrinth, resolving the pulsatile variations in flow caused by the action of the heart, was first made by visual observation and then using instrumental methods.
The tissues of the capillary plexus contain the same characteristic associations of Type I and Type II cells, together with nerve fibres, as are described in the carotid bodies of the Mammalia, and in the carotid labyrinths of other Amphibia. These associations, which are believed to represent chemoreceptor units, apparently have efferent synaptic complexes against the membrane of the Type I cell. The dense-cored vesicles within the Type I cells fall within the size range described for the other species. Similar characteristic cell groups, complete with nerve supplies, were also observed in the surrounding connective tissue. The carotid nerve contains about 15 myelinated and up to 150 fine (0.15-0.5µm) unmyelinated axons and leaves the sheath of the lingual ramus of the glossopharyngeal nerve through a ganglion of 25-40 cells. It supplies the labyrinth alone.
The capillary plexus tissue, in which the characteristic cells are dispersed, is a densely cellular connective tissue and provides a network of random channels for the throughflow of blood. Melanocytes, collagen and elastic fibres, and nerve fibres are embedded in the matrix. The organ is mechanically passive since the only smooth muscle is found as a thin layer in the proximal main chamber.
Blood flow measurements utilized the moving erythrocytes as tracers. Their movement, visible through the semi-transparent arterial walls, was recorded with a television camera and later analyzed with a microkymograph. Simultaneous recording of the ECG-related velocity measurements to the phase of the cardiac cycle. Flow in the common carotid was markedly pulsatile, entering the labyrinth in bursts and causing it to swell, while flow in the internal carotid was steady. Flow in the external carotid reversed for a large part of the cycle, returning to the roots of that vessel as the entire organ was distended. The organ owes its pulse-filtering behaviour to the resistive effect of the capillary plexus, combined with a reservoir-like storage due to the compliance of the fibroelastic capsule. This function concurs with Ask-Upmark's observation that all mammals have some pulse-filtering device interposed in their cranial arterial supply. I propose this to be the main function of the labyrinth, accounting adequately for its complex vascular structure. Its undoubted chemoreceptor function clearly can coexist happily with this vascular one.