Hearing in primitive fish

The question of how the sense of hearing and the vertebrate auditory system evolved has been a recurrent theme of investigators for many years (e.g. van Bergejk 1967, Wever 1974). The consensus among earlier investigators was that hearing achieves its highest form among birds and mammals.

Recently, we have began to reconsider issues related to the origin of several aspects of vertebrate hearing based on decades-long work on the auditory system of fishes. We suggest that many basic auditory functions evolved very early in vertebrate history, and that the functions observed in more “advanced” vertebrates, such as birds and mammals, are frequently modifications of themes first encountered in advanced fishes, and perhaps even more ancestral animals (see Popper and Fay 1997, Fay and Popper 2000) such as the “primitive fishes” (e.g. sturgeon, bichir, reedfish, gar, bowfin, shark, and lungfish).

We hypothesize that there may be a set of very general selective pressures that have shaped the functions of auditory systems throughout vertebrate evolution. The selective advantage may come from the ability to perform sound source determination and segregation (i.e. auditory scene analysis) that we assume has been important throughout the evolution of vertebrate hearing. This has led us to the further hypothesis that the auditory system in all vertebrates probably have very similar functional approaches to sound detection and analysis.

In order to test our hypothesis that basic hearing functions arose early in the evolution of fishes we are investigating hearing structure and function in the most “primitive” extant fishes that are more representative of taxonomic groups that have led to advanced fishes and the terrestrial vertebrates.

In order to test our hypothesis that basic hearing functions arose early in the evolution of fishes we are investigating hearing structure and function in the most “primitive” extant fishes that are more representative of taxonomic groups that have led to advanced fishes and the terrestrial vertebrates.

The first primitive genus we are using is the sturgeon, Acipenser. Sturgeon belong to the order Acipenseriformes which together with the Polypteriformes (bichir and reedfishes) form the group “lower Actinopterygian fishes”. It is assumed that the Acipenseriformes separated from the “advanced fishes” in the Triassic, about 200 million years ago. Because of their diversity and phylogenetic position as a basal group within Actinopterygians, Acipenseriformes are considered to be essential for comparative studies within extant and fossil Actiopterygians in the evolutionary literature.

We investigated frequency tuning and directional responses of single auditory nerve fibers in the lake sturgeon (Acipenser fulvescens) stimulated with a three axis shaker system. This system generated linear translatory motion along various axes in the horizontal and mid-saggitatl planes of the fish, thereby simulating acoustic particle motion. To test frequency responses, displacements were generated in the vertical plane and the frequency varied between 50 and 1000 Hz.

 
Figure 3. Isolevel frequency response functions in Acipenser fulvescens (auditory nerve recordings)
Figure 4. Directional response profiles for horizontal and vertical planes in Acipenser fulvescens (auditory nerve recordings)

Frequency data showed best responses (strongest degree of phase coupling or highest spike rate) at frequencies between 100 and 200 Hz (Fig. 3). Most units had cosine-shaped directional response profiles in the horizontal and mid-saggital planes (Fig. 4). Auditory nerve cells responded better to stimulus angles in the vertical plane rather than in the horizontal plane. The data show that auditory nerve fibers in sturgeon are frequency-tuned and directionally tuned which is very common in teleost fishes (modern bony fishes). The shape of the directional response profiles are also similar to those found in teleost fishes, indicating that the physiological mechanism encoding the direction of sound and the frequency of sound may have arisen very early in vertebrate history.

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