A unique swim bladder-inner ear connection in a teleost fish revealed by a combined high-resolution microtomographic and three-dimensional histological study

Background: In most modern bony fishes (teleosts) hearing improvement is often correlated with a close morphological relationship between the swim bladder or other gas-filled cavities and the saccule or more rarely with the utricle. A connection of an accessory hearing structure to the third end organ, the lagena, has not yet been reported. A recent study in the Asian cichlid Etroplus maculatus provided the first evidence that a swim bladder may come close to the lagena. Our study was designed to uncover the swim bladder-inner ear relationship in this species. We used a new approach by applying a combination of two high-resolution techniques, namely microtomographic (microCT) imaging and histological serial semithin sectioning, providing the basis for subsequent three-dimensional reconstructions. Prior to the morphological study, we additionally measured auditory evoked potentials at four frequencies (0.5, 1, 2, 3 kHz) to test the hearing abilities of the fish. Results: E. maculatus revealed a complex swim bladder-inner ear connection in which a bipartite swim bladder extension contacts the upper as well as the lower parts of each inner ear, a condition not observed in any other teleost species studied so far. The gas-filled part of the extension is connected to the lagena via a thin bony lamella and is firmly attached to this bony lamella with connective material. The second part of the extension, a pad-like structure, approaches the posterior and horizontal semicircular canals and a recessus located posterior to the utricle. Conclusions: Our study is the first detailed report of a link between the swim bladder and the lagena in a teleost species. We suggest that the lagena has an auditory function in this species because the most intimate contact exists between the swim bladder and this end organ. The specialized attachment of the saccule to the cranial bone and the close proximity of the swim bladder extension to the recessus located posterior to the utricle indicate that the saccule and the utricle also receive parallel inputs from the swim bladder extension. We further showed that a combination of non-destructive microCT imaging with histological analyses on the same specimen provides a powerful tool to decipher and interpret fine structures and to compensate for methodological artifacts.