124
theoretically provide robust and uniquely underwater binaural cues for sound
localization.
1.2 Fish Inner Ears and Modes of Hearing
The inner ear of fishes includes three semicircular canals that encode angular
momentum in each plane (vestibular function) and three otolithic end organs (saccule, lagena, and utricle) that may serve an auditory and/or vestibular (positional)
function (Platt and Popper 1981; Popper and Fay 1993). Each end organ has a
distinct pattern of sensory hair cell orientations that are arranged in different
planes, which provide the potential for three-dimensional encoding of the vector of
particle motion for sound source localization. Of the three otolithic end organs, the
saccule is the end organ most often implicated for use in hearing in teleost fishes
(Popper and Fay 1993). The possible acoustic functions of the utricle and lagena
are not well understood, but previous studies suggest that both the utricle and
lagena are capable of coding acoustic particle motion (Lu et al. 2003, 2004; Meyer
et al. 2010, 2012).
Fishes have evolved at least two modes of hearing: (1) a pressure-mediated
mode, found in derived teleost species (e.g., otophysans) with special morphological adaptations for transducing the pressure-induced vibrations of the swim bladder
to inner ear acoustic end organs (e.g., Weberian ossicles or gas-filled vesicles in
close proximity to the inner ear) that can be used to enhance pressure detection
although some fish (e.g., the cod and midshipman) can sense acoustic pressure from
pressure-induced swim bladder vibration even in the absence of any special morphological adaptations (Sand and Enger 1973; Chapman and Sand 1974; Tytler and
Blaxter 1977) and (2) an inertial mode, thought to be shared by all fishes, which
results from the relative motion of the high-density otoliths and underlying sensory
hair-cell epithelium in the inner ear end organs due to acoustic particle motion (de
Vries 1950; Popper and Fay 1993). The inner ear end organs essentially function as
inertial accelerometers, and thus respond to acoustic particle motion (de Vries 1950;
Dijkgraaf 1960; see above). In this ancestral inertial mode of hearing, the fish’s
body moves with the same displacement, direction, and phase as water due to similar acoustic properties (i.e., the fish has little or no difference in impedance to that
of water). However, because otoliths are denser than water, they move with smaller
amplitude and lag in phase relative to the fish’s body, which results in the net movement of the otolith relative to the sensory macula and results in the deflection of the
end organ’s hair cells in the sensory macula (Fig. 1). At the level of the hair cell, the
deflection of the hair bundle toward the longest cilium, caused by particle motion
along the axis to which the hair bundle is intrinsically “tuned” (by its geometry),
leads to hair cell depolarization and the release of excitatory neurotransmitter.
Sufficient neurotransmitter release initiates action potentials in the innervating primary auditory afferents that then propagate via the VIIIth cranial nerve to the auditory hindbrain and central auditory pathway. Hair cells are inherently directionally
J.A. Sisneros and P.H. Rogers
theoretically provide robust and uniquely underwater binaural cues for sound
localization.
1.2 Fish Inner Ears and Modes of Hearing
The inner ear of fishes includes three semicircular canals that encode angular
momentum in each plane (vestibular function) and three otolithic end organs (saccule, lagena, and utricle) that may serve an auditory and/or vestibular (positional)
function (Platt and Popper 1981; Popper and Fay 1993). Each end organ has a
distinct pattern of sensory hair cell orientations that are arranged in different
planes, which provide the potential for three-dimensional encoding of the vector of
particle motion for sound source localization. Of the three otolithic end organs, the
saccule is the end organ most often implicated for use in hearing in teleost fishes
(Popper and Fay 1993). The possible acoustic functions of the utricle and lagena
are not well understood, but previous studies suggest that both the utricle and
lagena are capable of coding acoustic particle motion (Lu et al. 2003, 2004; Meyer
et al. 2010, 2012).
Fishes have evolved at least two modes of hearing: (1) a pressure-mediated
mode, found in derived teleost species (e.g., otophysans) with special morphological adaptations for transducing the pressure-induced vibrations of the swim bladder
to inner ear acoustic end organs (e.g., Weberian ossicles or gas-filled vesicles in
close proximity to the inner ear) that can be used to enhance pressure detection
although some fish (e.g., the cod and midshipman) can sense acoustic pressure from
pressure-induced swim bladder vibration even in the absence of any special morphological adaptations (Sand and Enger 1973; Chapman and Sand 1974; Tytler and
Blaxter 1977) and (2) an inertial mode, thought to be shared by all fishes, which
results from the relative motion of the high-density otoliths and underlying sensory
hair-cell epithelium in the inner ear end organs due to acoustic particle motion (de
Vries 1950; Popper and Fay 1993). The inner ear end organs essentially function as
inertial accelerometers, and thus respond to acoustic particle motion (de Vries 1950;
Dijkgraaf 1960; see above). In this ancestral inertial mode of hearing, the fish’s
body moves with the same displacement, direction, and phase as water due to similar acoustic properties (i.e., the fish has little or no difference in impedance to that
of water). However, because otoliths are denser than water, they move with smaller
amplitude and lag in phase relative to the fish’s body, which results in the net movement of the otolith relative to the sensory macula and results in the deflection of the
end organ’s hair cells in the sensory macula (Fig. 1). At the level of the hair cell, the
deflection of the hair bundle toward the longest cilium, caused by particle motion
along the axis to which the hair bundle is intrinsically “tuned” (by its geometry),
leads to hair cell depolarization and the release of excitatory neurotransmitter.
Sufficient neurotransmitter release initiates action potentials in the innervating primary auditory afferents that then propagate via the VIIIth cranial nerve to the auditory hindbrain and central auditory pathway. Hair cells are inherently directionally
J.A. Sisneros and P.H. Rogers