The inner ear of the lungfish Protopterus

Abstract

The sensory end organs of the inner ear of the lungfish, Protopterus, were examined using scanning and transmission electron microscopy. The utricle has a structure and hair cell orientation pattern that are typical for vertebrates, although the hair cells are unusually large. There are the typical three semicircular canals extending from the utricle, with the typical hair cell orientations, but the lateral canal sensory crista looks like the "hemicrista" of some amphibians and amniotes, lacking a saddle-shaped flare on one wall of the ampulla. Unlike most vertebrates that have the saccule and lagena as two separate pouches ventral to the utricle, the lungfish has a single large ventral pouch that contains a single large pasty otoconial mass. This mass covers two hair cell patches, each like a striola with prominent hair cell ciliary bundles, that are presumed to represent saccular and lagenar maculae. However, these two major sensory patches are not completely separate maculae because they lie within a less densely populated field of smaller hair cells, which forms an extrastriolar region that surrounds and fills the region between the two striolae of higher hair cell density. The more caudal lagenar striola is a vertically elongated stripe with hair cell orientation vectors facing antiparallel on either side of a midline drawn vertically along the macula, resembling the macula lagena of some bony fishes but not of tetrapods. The more rostral saccular striola is a curving band with hair cell orientation vectors facing away from its midline, but because this macula curves in three dimensions, the vectors at the rostral end of this striola are oriented mediolaterally, whereas the vectors on the caudal half of this striola are oriented dorsoventrally. The presence of a macula neglecta was confirmed near the posterior canal as a tiny single patch of a few dozen hair cells with all the cell orientations directed caudally. The ciliary bundles on the cells in the striolar-like regions of all of three otolithic organs average over 80 cilia, a number far greater than for any other fish studied to date. The features of the single sacculolagenar pouch with separate striolar-like regions, the cellular orientation in the otolith organs, and the large cells and ciliary bundles in Protopterus also were observed in specimens of the other extant lungfish genera, Lepidosiren and Neoceratodus.

Hearing in the African lungfish ( Protopterus annectens ): pre-adaptation to pressure hearing in tetrapods?

“…For example, Fritzsch [16] has proposed that the basilar papilla in frogs should be homologous to an area in the inner ear of the coelacanth. This hypothesis would agree with scenario 1, but the evidence for homology is weak [7].…”

Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology

“…In all cartilaginous fishes and some members of the Actinopterygii, a fourth macula, namely the macula neglecta, is present (Casper, 2011). It consists of one or two small patches housing several dozen (e.g., Platt et al, 2004) up to thousands of sensory hair cells (e.g., Corwin, 1981). Similar to the canal cristae, the macula neglecta is overlain by a gelatinous cupula and lacks otoconia or an overlying otolith.…”

“…In Holocephali (Retzius, 1881;de Burlet, 1934), lungfishes (Retzius, 1881;Platt et al, 2004), and non-actinopterygian teleosts (Popper, 1978;Popper and Northcutt, 1983;Mathiesen and Popper, 1987;Lovell et al, 2005) saccule and lagena form one pouch, whereas in the coelacanth Latimeria (Fritzsch, 1987(Fritzsch, , 2003, elasmobranchs (e.g., Retzius, 1881;Ladich and Popper, 2004), and teleosts (e.g., Ladich and Popper, 2004;Popper and Schilt, 2008) these otolith end organs form two interconnected sacs. The saccule is often the largest of the three otolith end organs ( Figures 1A-B, 2B-E), with teleost orders including Gobiiformes (Figure 2C; e.g., Retzius, 1881;Popper, 1981), Ophidiiformes (e.g., Parmentier et al, 2001Parmentier et al, , 2002Kéver et al, 2014), and Batrachoidiformes (e.g., Cohen and Winn, 1967) representing members with one of the largest saccules compared to the tiny utricle and lagena.…”

“…In lungfishes, the macula sacculi and macula lagenae form a continuum, the so-called sacculolagenar macula in which two regions of high hair cell densities (striolas) are separated by areas of lower hair cell densities (Figures 1C, 6C; Platt et al, 2004). Such a sacculolagenar macula is unique among bony fishes.…”

“…The maculae in (E-H) stem from species that possess accessory hearing structures. Illustrations modified from Barber and Emerson (1980), Deng et al (2013), Mathiesen and Popper (1987), Platt (1977), Platt et al (2004), Popper (1978), Popper and Platt (1979), Popper and Tavolga (1981), and Schulz-Mirbach et al (2014). a, anterior;d, dorsal;lat, lateral. modified orientation patterns.…”