The anatomy and ultrastructure of the labyrinth of the lamprey ( Lampetra fluviatilis L.)

Abstract

The anatomy of the labyrinth of the lamprey ( Lampetra fluviatilis ) is described. The am­pullae of the two semicircular canals are each equipped with a complex three-armed sensory crista. They may be considered homologues of the ampullae of the vertical canals of the gnathostomes. However, the complexity of their cristae encourages the assumption that they may cover a spatial range of responses to angular acceleration which includes responses to accelerations in a horizontal plane controlled in the gnathostomes by the horizontal semi-circular canal. The otolith-bearing end organs are found to be located on a common macular structure. This is subdivided into an anterior horizontal, a vertical, and a posterior horizontal macula, each of which portions carries a characteristic arrangement of sensory cells. On the basis of an electronmicroscopic analysis of the orientation of the hair cells in the three main portions of the macula a revision of the homologies found in the older literature appears to be called for. It is suggested to homologize the anterior horizontal macula with the macula utriculi, the vertical macula with the macula sacculi and the posterior horizontal macula with the macula lagenae of the labyrinth of gnathostome animals. A separate sensory ending in the dorsal part of the labyrinth, the dorsal macula, may be the homologue of the macula neglecta. Ultrastructurally the end organs of the lamprey labyrinth conform with those of the gnathostome labyrinth with the exception of the presence of a new type of sensory hair cell which is equipped with a stiff kinoeilium of extraordinary length accompanied by extremely short stereocilia. This cell is found preponderantly in the vertical macula (macula sacculi). A striated organelle in the cytoplasm of the hair cells appears to be uniquely confined to the labyrinth of the lamprey. Morphologically the lamprey labyrinth differs from all other chordate labyrinths including that of its fellow cyclostome Myxine by the presence of large ciliated chambers in its centre in which long and powerful cilia maintain a permanent pattern of four endolymph vortices. The ciliated chambers are in open communication with the ampullae and with the spaces con­taining the otolith-bearing maculae. The analysis of the functional significance of the anatomical and ultrastructural findings will be described in a separate paper.

The developing lamprey ear closely resembles the zebrafish otic vesicle:otx1expression can account for all major patterning differences

“…1). Adult lamprey inner ears have only two semicircular canals, each with a tricuspid crista, and a single ventrally positioned macula communis that covers the floor of two joined, symmetrical, ciliated chambers (de Burlet and Versteegh, 1930;Lowenstein et al, 1968;Thornhill, 1972;Avallone et al, 2005). A similar pattern, with two semicircular canals, is found in the abundant agnathan fossil record, making it likely that this represents the ancestral condition (Mazan et al, 2000).…”

“…Hagfish also have a single macula communis on the ventral floor of the inner ear, but differ in having a single toroidal semicircular canal, which nevertheless is associated with two cristae, and is probably a derived characteristic (Lowenstein and Thornhill, 1970) (for a review, see Lowenstein, 1971). Although the general appearance of the inner ear is symmetrical about the AP axis in adult agnathan fishes, the macula communis can be subdivided into at least three morphologically distinct regions, the anterior horizontal, vertical and posterior horizontal regions (Lowenstein et al, 1968;Lowenstein and Thornhill, 1970;Hagelin, 1974), and there have been several different interpretations of the homology of these regions to the various gnathostome maculae (de Burlet and Versteegh, 1930;Lowenstein et al, 1968;Thornhill, 1972;Hagelin, 1974). Several studies describe hair cell planar polarity patterns in the late larval and adult lamprey and hagfish macula communis as roughly symmetrical about the AP axis (Lowenstein et al, 1968;Lowenstein and Thornhill, 1970;Thornhill, 1972), and Hagelin (Hagelin, 1974) tentatively proposes that both the anterior and posterior ends of the lamprey macula correspond to the gnathostome utricular macula.…”

Structure and function of the Nautilus statocyst

“…In all coleoid cephalopods, the cilia in the canal are known to be motile (Budelmann 1988). In vertebrates, a similar canal-like opening to the exterior is known in the vestibular organ of lampreys and some elasmobranchs; its multi-ciliated epithelial cells are described as non-innervated and their cilia as motile (Löwenstein et al 1968;Löwenstein 1974;Popper & Hoxter 1987).…”

Ultrastructural observations of efferent terminals in the crista Ampullaris of the toadfish, opsanus tau

“…However, there is increasing evidence for the existence of a multiplicity of morphologically defined hair cell types in anamniotes (Popper 2000). Although early ultrastructural studies did indeed demonstrate the existence of morphologic variations in the hair cells of bony fishes (Flock 1964;Lowenstein et al 1968;Wegner 1982), the demonstration that these might not all be variants of mammalian type II cells is more recent (Saidel and Presson 1990;Chang et al 1992;Lanford and Popper 1996;Saidel and Crowder 1997) and suggests that a revision of the classic scheme is in order. Synapses between hair cells and primary afferents occur at morphologically discrete contacts that are often distinguished by the presence of a synaptic body with a halo of electron-lucent vesicles in the receptor cell, and a postsynaptic density associated with the afferent terminal membrane (Sans and Highstein 1984).…”