Hearing in Primitive Fishes

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.

Former graduate student Dr. Michaela Meyer (co-advised by Dr. Arthur N. Popper and Dr. Richard R. Fay), wanted 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” or “modern” 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” (or “ancestral”) bony fishes (e.g., sturgeon, bichir, reedfish, gar, bowfin, shark, and lungfish). Studies have shown that the morphology of the inner ear of several ancestral bony fish species have remarkable similarities to the morphology of modern bony fishes or teleosts (Popper 1978, Mathiesen and Popper 1987, Popper and Northcutt 1983, Platt et al. 2004, Jorgensen and Popper 2010).

In her dissertation, Dr.Meyer focused on two major mechanisms important for hearing: spectral analysis, the decomposition of sound into its frequency components, and sound source localization. The encoding of sound frequency, intensity, and directionality by fish auditory nerves, that innervate the inner ear, have been studied in a few modern bony fish species (e.g., Moeng and Popper 1984, Fay 1984, Fay and Ream 1986, Fay and Edds-Walton 1997,Lu et al. 1998, McKibben and Bass 1999). These findings from teleost species provided the platform to which to compare data from an ancestral bony fish species.

Dr. Meyer decided on using the sturgeon (Acipenseridae) as a representative ancestral bony fish family, since this group contains the largest number of ancestral bony fish species that still exists on earth. For comparison: there are only 48 extant ancestral bony fish species total vs. over 26,000 species of modern bony fish species (teleosts). Twenty five of the ancestral species belong to sturgeon. The species used, was the lake sturgeon, which occur in fresh water of North America and Canada and usually live on the bottom of the riverbed or lake. These fish can migrate up to 200 km to find a suitable habitat for spawning in rivers.  

To investigate frequency and directional responses of eighth nerve afferents innervating the saccule and lagena, we used a shaker system (Fay 1984), which moved the fish along various directions in the vertical and horizontal planes at different frequencies and intensities. During stimulation, we recorded from the eighth nerve innervating the saccule or lagena of the lake sturgeon.

Many physiological characteristics resembled data found in teleosts: background activity of fibers varied and showed different firing pattern (regular, irregular, bursting). Responses to linear acceleration showed strong phase-coupling and a wide range of thresholds spanning at least 60 dB re 1 nm displacement). Fibers also differed in their best frequency (BF), sharpness of tuning, and in the shape of the frequency function – just as seen in telelosts. Best frequencies occurred between 100 and 300 Hz (Fig. 1) with the majority of fibers having their BF at 100 or 141 Hz. Directional response profiles resembled cosine functions occurring at a wide range of stimulus intensities. However, best axes of most fibers (76%) did not respond to horizontal stimulation (Fig. 2A) and responded best to movements near 90◦ in the vertical plane (up down; 76%; Fig. 2B). Sixty-two percent of afferents responsive to horizontal stimulation had their best axis in azimuth near 0◦ (front back). In summary, many basic physiological characteristics typical for the encoding of sound in teleosts and other vertebrates have been found in sturgeon. However, coding for sound direction in the vertical and horizontal planes seemed to be limited or lake sturgeon may be using different strategies for encoding a sound source than teleosts.

Fig. 1: Example of a typical frequency response of one fiber (single unit) in lake sturgeon. The left graph represents an isolevel frequency response: here the response strength (Z) is plotted as a function of frequency for different levels (see inset); the right graph represents a contour plot of the same data. The color code to the right of the contour plot indicates the response strength (Z-value). The best frequency of this fiber was 141 Hz, the best direction was 90◦ vertical and no response to horizontal plane stimuli occurred (frequency responses were obtained at the best direction).

Fig. 2: Example of a typical directional response profiles of one fiber (single unit) to stimuli in the horizontal (A) and vertical plane (B) in lake sturgeon. Each data point represents the response strength of the fiber (Z-value) and was obtained at a particular stimulus direction the fish was moved along. Measurements have been obtained at the best frequency of the fiber (100 Hz) and were repeated at four different levels (see inset).

We may hypothesize that the results from sturgeon constitute the ancestral condition in terms of the similarities of the physiological and ear morphology in teleosts. Regarding directional preferences, lake sturgeon could also have adapted to a particular ecological niche that leads to a constrained ability (focus on top down information) for sound source localization. More data are needed to further assess ancestral versus modern strategies for sound encoding using different species of non-teleost bony fishes as well as species of the outgroup of bony fishes, the cartilaginous fish (sharks and rays).

Publications:  

Popper, A.N. (1978). Scanning electron microscopic study of the otolithic organs in the bichir (Polypterus bichir) and shovel‑nose sturgeon (Scaphirhynchus platorynchus). J. Comp. Neurol. 18:117‑128. https://doi.org/10.1002/cne.901810107

Meyer, M., Fay, R. R., and Popper, A. N. (2010). Frequency tuning and intensity coding of sound in the auditory periphery of the lake sturgeon, Acipenser fulvescens. Journal of Experimental Biology, 213:1567-1578. Link

Meyer, M., Popper, A. N., and Fay, R. R. (2012). Coding of sound direction in the auditory periphery of the lake sturgeon, Acipenser fulvescens. Journal of Neurophysiology., 107:658-665. Link

Jorgensen, J. M. and Popper, A. N. (2010). The inner ear of lungfishes. In: Jorgensen, J. M. and Joss, J., (eds.) The Biology of Lungfishes. Pp. 489-498. CRC Press, Boca Raton, FL.