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.
Meyer, M., Popper, A. N., and Fay, R. R. (2012).
of sound direction in the auditory periphery of the lake sturgeon,
Journal of Neurophysiology., 107:658-665.
Jørgensen, J. M.
and Popper, A. N. (2010). The inner ear of lungfishes. In:
Jørgensen, J. M. and Joss, J., (eds.)
The Biology of
Lungfishes. Pp. 489-498. CRC Press, Boca Raton,
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, Jørgensen and
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.
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).