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First published online May 1, 2009
Journal of Experimental Biology 212, 1483-1493 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.026898
Physiological evidence for binaural directional computations in the brainstem of the oyster toadfish, Opsanus tau (L.)
1 Parmly Hearing Institute, Loyola University Chicago, Chicago, IL 60626,
USA
2 Neuroscience Institute, Marine Biological Laboratory, Woods Hole, MA 02543,
USA
* Author for correspondence (e-mail: plewalton{at}yahoo.com)
Accepted 23 February 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: auditory, descending octaval nucleus, torus semicircularis, directional hearing
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Sound localization by terrestrial vertebrates requires binaural comparisons
(for reviews, see Brown and May,
2005; Christensen-Dalsgaard,
2005; Trahiotis et al.,
2005), beginning with parallel neural pathways that encode small
acoustic time of arrival differences and sound level differences. In water,
the speed of sound is about five times faster than in air, making interaural
time differences five times shorter underwater than in air for a vertebrate of
similar head size. In addition, the fish's ears are relatively close together
physically, and the skull is surrounded by tissue that is approximately the
same density as water. Therefore, acoustic cues for interaural time
differences (ITD) and interaural level differences (ILD) are expected to be
very small or non-existent, and the binaural processing mechanisms typical of
terrestrial vertebrates would not be sufficient to detect those minute
differences. However, there are multiple lines of evidence indicating that
directional hearing in fishes involves binaural processing and that interaural
comparisons could be present in the directional hearing pathway of fishes
(reviewed by Fay, 2005).
Sound has both a kinetic, particle motion component, and a pressure
component. In fishes, the axis of acoustic particle motion is encoded by the
variously oriented sensory hair cells on the otolithic endorgans of the ear
(Sand, 1974;
Hawkins and Horner, 1981;
Fay, 1984;
Fay and Edds-Walton, 1997a;
Fay and Edds-Walton, 1997b;
Edds-Walton et al., 1999;
Lu at al., 1998). Each
endorgan has a sensory epithelium and calcareous otolith, which together
function like an inertial accelerometer (de
Vries, 1950). The hair cells on the epithelium are anatomically
specialized neurons with mechanically activated surface structures that are
physiologically polarized with a `best axis'
(Flock, 1964). Particle motion
along the best axis maximally excites the hair cell. Particle motion
perpendicular to that axis causes a null in neural activity, and excitation at
other angles causes a graded response that is proportional to a cosine
function of the angle of particle motion with respect to the hair cell's best
axis. In most fishes, auditory hair cells are activated by particle motion
between about 50 and 1000 Hz. There are three otolithic endorgans in teleost
fishes that may have auditory response characteristics (saccule, lagena and
utricle). Research on a variety of fish species indicates that the saccule is
the greatest contributor to auditory processing in most fishes
(Fay, 2005).
Sand (Sand, 1974) recorded
microphonic potentials from left and right ears of a perch (Perca
fluviatilis, Linnaeus) in response to oscillations of the fish in the
horizontal plane and showed that the two saccules responded with slightly
different directional response patterns. Sand hypothesized that interaural
comparisons would be sufficient to determine sound source direction in the
horizontal plane. Schuijf (Schuijf,
1975) provided early behavioral evidence that two ears were
necessary for cod (Gadus morhua, Linnaeus) to discriminate between
two different sound source locations. Using the same species, Horner and
colleagues (Horner et al.,
1980) provided physiological evidence that binaural auditory
processing sites were present through unilateral and bilateral electrical
blockage of input from the saccule, which resulted in reduction or elimination
of auditory responses in the medulla and the midbrain.
Our lab (Edds-Walton et al.,
1999) has shown that auditory afferents from the saccule of the
toadfish (Opsanus tau, Linnaeus) contact multiple hair cells that
have similar or identical best directions. The direction of stimulation is
transmitted via primary afferents in cranial nerve VIII to the
descending octaval nucleus (DON) in the medulla
(Edds-Walton and Fay, 1998;
Edds-Walton and Fay, 2008).
Both the left and right DONs project to the midbrain torus semicircularis (TS)
where directional information is retained
(Wubbels and Schellart, 1998a;
Wubbels and Schellart, 1998b;
Wubbels et al., 1995;
Ma and Fay, 2002;
Edds-Walton and Fay, 2003) and
enhanced directionality (directional sharpening) is common
(Edds-Walton and Fay, 2005a).
Thus, encoding the axis of particle motion for audio frequencies is one of the
consistent functions of the ascending auditory pathway in the toadfish. We
have hypothesized that binaural computations could account for the wide range
of best axes and directional sharpening documented in the torus semicircularis
of toadfish (Edds-Walton and Fay,
2003).
Anatomical tract-tracing studies consistently show that the auditory
midbrain receives input from first-order and second-order auditory nuclei in
the left and right auditory medulla in a variety of teleost fishes (reviewed
by McCormick, 1999). In
addition, Edds-Walton (Edds-Walton,
1998) demonstrated a commissural tract carrying axons between the
DONs in toadfish. Therefore, both the DON and TS have the neural basis for
interaural comparisons, but binaural response characteristics indicative of
directional auditory processing have not been confirmed anywhere along the
ascending auditory pathway of a fish.
In this paper we will describe further physiological evidence that convergence of left and right directional inputs occurs in the DON and TS of the toadfish. Using a new, readily reversible technique, we show that manipulating the contralateral saccular otolith can change the responsiveness of a cell in the DON or in the TS. These data indicate that binaural mechanisms play a role in the neural representation of direction in the brainstem of the toadfish.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), but also includes the divisions of the DON described in
O. beta (Bass et al.,
2001). The DON lies within the octaval column, between the
entrance of cranial nerves VIII and X. Near the anterior ramus of VIII, the
ventro-lateral DON transitions into the tangential octaval nucleus and the
dorso-lateral DON transitions into the magnocellular octaval nucleus. The
dorso-medial division appears near VIII and transitions into the dorsal
secondary octaval nucleus medially. In order to limit recordings to the DON,
recording sites were restricted rostro-caudally to the area between the
posterior ramus of VIII and IX. The presence of a large blood sinus prevented
access to the dorso-medial division of the DON.
A preliminary investigation of auditory sites in the DON was conducted
using neurobiotin injections following characterization of an auditory unit.
Those studies were conducted prior to commencement of the present experiments
involving otolith manipulations (described below). Neurobiotin was injected
into the medulla via positive current (1600–2000 nA) from the
recording electrode for 20–30 min. The surgical opening was sealed and
the fish placed in aerated seawater for label transport to occur over
8–12 h. The toadfish then was anesthetized and perfused through the
ventricle with buffered toadfish saline followed by perfusion with fixative
(4% paraformaldehyde in 0.1 mol l–1 PBS). The brain was
excised and postfixed for 1 h, rinsed and refrigerated in PBS overnight. The
brain was cryoprotected by infusion of 40% sucrose over 24 h, embedded in
Tissue-Tek OCT, and sectioned (50 µm). The neurobiotin was visualized in
floating sections using a standard ABC-DAB reaction (Elite kit, Invitrogen,
Carlsbad, CA, USA) with metal intensification (modified from
Hancock, 1982). The sections
were stored in buffer until mounted onto gelatin-coated slides, dehydrated
through alcohols, cleared in Citrisolv (Fisherbrand, Pittsburgh, PA, USA) and
cover-slipped for examination on an Olympus BX50 with drawing tube and digital
camera (DP12 camera system: Olympus, Center Valley, PA, USA).
Our previous anatomical and physiological work in the DON and the TS
allowed us to visually define appropriate recording sites
(Edds-Walton, 1998;
Edds-Walton et al., 1999;
Edds-Walton and Fay, 1998;
Edds-Walton and Fay, 2003;
Edds-Walton and Fay, 2005a;
Edds-Walton and Fay, 2005b;
Edds-Walton and Fay, 2008).
Small neurobiotin injections (1600–1900 nA, 10–15 min) were used
to confirm the recording site in some fish (N=15). For those cases,
physiological recording ceased after the injection, and the fish was prepared
for histological examination of the tissue (see above). Details of injection
methods and illustrations have been published previously
(Edds-Walton and Fay, 2003;
Edds-Walton and Fay, 2008).
Recording sites were not labeled in the midbrain during this study because the
location and physiology of auditory cells in the TS (nucleus centralis) have
been investigated in detail in a previous study
(Edds-Walton and Fay, 2005a;
Edds-Walton and Fay, 2005b).
During the search for auditory units in the midbrain, the recording electrode
traverses areas with predictable neural activity or lack thereof (e.g. the
ventricle). The auditory TS lies immediately below the ventricle, and no other
auditory sites could be encountered.
Electrophysiology and stimuli
Pulled, broken glass electrodes (5–20 M
) were used for
extracellular recordings of individual units in the DON and TS (Sutter
Instruments, Novato, CA, USA). Electrodes were filled with 3 mol
l–1 NaCl or 2 mol l–1 NaCl with 4%
neurobiotin (Invitrogen) for labeling recording sites, as described above.
All electrophysiology was conducted in the particle motion stimulus system
(shaker dish) designed by R.R.F. and used for all previous hearing research on
toadfish. Briefly, the fish was positioned in a custom-designed head-holder
attached to the edge of the dish. The dish contained local seawater up to the
level of the opening in the skull. A 50 ml syringe was used to remove and
replace water in the dish as needed to maintain appropriate temperature and
oxygenation. Particle motion was produced in the horizontal plane by two pairs
of mini-shakers (Bruel and Kjaer, Odense, Denmark) positioned back–front
and left–right of the fish, and in the mid-sagittal plane by the
front–back paired mini-shakers and a vertical shaker (Bruel and Kjaer).
Dish movement caused the fish to experience particle motion directly. A
diagram and detailed description of the apparatus were provided in our earlier
publication (Fay and Edds-Walton,
1997a). Three orthogonally positioned accelerometers (PCB
Piezotronics, Depew, NY, USA) mounted on the outer surface of the dish
monitored movement and were used to calibrate all directional and frequency
stimuli prior to each experiment to ensure consistency over the 4 years of
data collection.
The stimuli (500 ms; 20 ms rise and fall times) were presented in preprogrammed order at the designated level (dB re: 1 nm) with eight repetitions. Spike times were recorded with 0.1 ms resolution (Tucker-Davis Technologies, Gainesville, FL, USA), and the spike rate data were used to plot iso-level directional response patterns (DRPs) and iso-level frequency response curves. The DRPs were used to evaluate the best axis (most excitatory) in azimuth and in elevation prior to, during and following experimental manipulation of the otolith whenever possible (see below). Phase locking (how consistently the cell produces spikes at a particular phase of the sinusoidal stimulus) and the phase angle of the response were also recorded. Background activity was recorded in the absence of deliberate stimulation.
The response of cells to particle motion was evaluated at 30 deg. intervals
in the horizontal and mid-sagittal planes at 100 Hz, an appropriate frequency
for the broadly tuned auditory units in toadfish based on previous
experimentation (Fay and Edds-Walton,
1997b; Edds-Walton and Fay,
2008). In addition, the frequency response was evaluated at the
same frequencies used in our previous studies of the DON and TS (50, 65, 84,
100, 141, 185, 244, 303 Hz) with a stimulus angle of 30 deg. azimuth to the
left (0 deg. elevation) or 30 deg. elevation (0 deg. azimuth). The frequency
response functions were used during these experiments to help confirm that the
data obtained were from the manipulated cell, and not the activity of an
adjacent cell. Stimuli were presented at 5 dB increments in a sufficient range
of levels to evaluate the cell's sensitivity and generate data for the
DRP.
Surgery and otolith manipulation
The care and use of toadfish were approved by the Animal Care and Use
Committees at the Marine Biological Laboratory and Loyola University of
Chicago. For all surgical procedures the gills of the fish were washed with
buffered seawater containing MS222 (3-aminobenzoic acid methane-sulfonate
salt, 1:1000, pH 7.4; Sigma-Aldrich, St Louis, MO, USA) until opercular
movements ceased. Fish were paralyzed with an intramuscular injection of
pancuronium bromide (0.05 mg kg–1; Sigma-Aldrich) and placed
in a Plexiglas enclosure with aerated sea water. Lidocaine (Henry Schein,
Melville, NY, USA) was applied to the skin, a rectangular incision was made
dorsally, and the skin reflected. The muscle was removed and the skull was
opened to expose the medulla or midbrain. Intracranial fluids were replaced
with a fluorocarbon plasma substitute (FC-77, 3M Corp. Minneapolis, MN, USA)
to provide a clearer view. The bone of the midline suture was removed and the
triangular dura was peeled caudally to permit access to both sides of the
brain, taking great care to avoid a major dorsal vessel that descends from the
cranium and divides repeatedly to supply the midbrain.
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The saccule is located within the translucent membranous labyrinth of the
ear and is bathed in endolymph. The large, calcareous otolith lies adjacent to
the brainstem, where it is easily observed without surgical modification of
the area (Fig. 1A). The
saccular epithelium lies within a small central depression on the medial
surface of the otolith [see figure
1 in Edds-Walton et al.
(Edds-Walton et al., 1999)]
and is not visible without additional surgery. Therefore, we could not
evaluate the condition of the saccular epithelium directly, but inferred its
condition based on the consistency of data acquisition.
After the fish had been secured in the shaker dish, two or three 3-D
micromanipulators were positioned on opposite sides of the fish. One
micromanipulator held the recording electrode and ground. The second (and
third) micromanipulator held the hand-made tipper: a borosilicate micropipette
or synthetic electrode filler (World Precision Instruments, Sarasota, FL, USA)
attached to a 1 ml syringe. The tipper was positioned just above the dorsal
edge of the right (contralateral) and/or left (ipsilateral) saccular otolith
(Fig. 1A). The saccule was
chosen for manipulation for several reasons. First, we have characterized the
directional auditory responses from the saccule in this species and know that
it projects heavily to the auditory region of the DON. In addition,
experiments by Schuijf and Siemelink
(Schuijf and Siemelink, 1974)
revealed that surgical elimination of input from one saccule (and possibly the
lagena) impaired the ability of a cod to orient to a sound source at different
locations in azimuth, in the presence of intact utricles. The toadfish ear is
organized similarly to that of the cod, and there is no physiological evidence
to date that either the utricle or the lagena contribute to directional
hearing in either species.
All stimuli were presented prior to tipping the otolith to obtain a normal, pre-tipping DRP and frequency response at two to three different levels. Then gentle pressure was applied to the dorsal edge of the saccular otolith to tip the saccule away from the brain and alter the normal orientation of the sensory epithelium without damaging the labyrinth (Fig. 1A,B). Care was taken to ensure that the saccular nerve was not strained, which could alter normal neural activity. In general, the vertical orientation of the otolith edge was altered by 20–30 deg. All of the stimuli were presented again to obtain DRP and frequency response at two to three levels during tipping. Lastly, the tipper was retracted slowly by reversing the micromanipulator. In most cases, a 5–10 min recovery period was permitted prior to the post-tipping repetition of the stimuli, again at two to three levels. In all cases, post-tipping data were collected to confirm that tipping had not permanently altered the response of the unit under study. If the unit did not respond post-tipping, the unit was considered lost, and the data were eliminated from further consideration.
The experimental procedures were identical for recordings in the DON and in the TS. The contralateral otolith was tipped in the majority of the experiments reported here. In a few fish, the skull was large enough to permit the use of two tippers, one that targeted the ipsilateral saccular otolith and a second that targeted the contralateral otolith while the recording electrode was placed in the DON. However, the probe was applied sequentially, not simultaneously, to each side, due to space limitations. Sequential tipping was usually done only if contralateral tipping was unsuccessful. There was never sufficient space to allow simultaneous ipsilateral and contralateral tippers with the recording electrode located in the midbrain.
Tipping was employed as an easily reversible method of temporarily altering the orientation of the saccule, although it did not produce predictable results with every application of the tipper. In preliminary experiments, we showed that tipping the ipsilateral saccular otolith caused consistent reductions in multi-unit activity in the DON (Fig. 2). However, in subsequent recordings from single units, tipping the ipsilateral otolith did not always produce a change in the DON cell's activity (e.g. Fig. 3). There are two potential explanations for the lack of an effect: (1) the DON cell did not receive auditory input from the ipsilateral saccule or (2) the saccular inputs to that particular DON cell were not affected by tipping because all regions of the saccular epithelium are not affected equally by tipping. Of these two possibilities, we believe the second is the most likely reason for a lack of change in the DRP during ipsilateral tipping. Based on the ipsilateral otolith tipping experiments, the lack of a change in the DRP of a DON cell during contralateral otolith tipping cannot be interpreted as evidence that the cell does not receive contralateral input. Similarly, tipping did not always affect the responsiveness of TS cells (Fig. 3), but altered responses were obtainable with this method. We will focus on the cases in which we were able to obtain a reversible change in the spike rate or shape of the DRP of a unit in the DON or the TS during tipping of the contralateral saccular otolith. To be included in this data set, we required complete directional data at two stimulus levels with consistent DRPs.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) that
identified a commissural connection between the left and right DONs and
support the hypothesis that binaural auditory cells are likely to be present
in the DON of toadfish. The locations of cranial nerves VIII and IX are dependable landmarks for the rostro-caudal extent of the DON. Neurobiotin injections were limited to maximize use of each fish, as fish had to be killed immediately after injection to prevent label transport from the injection site. Neurobiotin was injected only when a recording site was at the extremes of the desired recording area, e.g. particularly rostral, medial or deep (N=15). Three data sets were eliminated due to the location of the injection in an adjacent nucleus. No injections were placed in the midbrain. Our previous work in the TS provided sufficient experience and confidence of location when recording auditory activity.
Responses to tipping
For brevity, the simple term tipping will be used to indicate that the
saccular otolith was tipped, and either ipsi (ipsilateral) or contra
(contralateral) will indicate which saccular otolith was tipped with respect
to the recording site. The presence of binaural input was evaluated in 70 left
DON auditory units, and 30 left and one right TS auditory unit. Of the
experiments in the DON, 21 were ipsi tipping, 42 were contra tipping, and
seven were sequential tipping of the contra and ipsi saccular otoliths. The TS
tipping experiments consisted of two ipsi, 29 contra and a single sequential
tipping.
The ipsilateral tipping experiments conducted while recording in the DON
validated the repeatability of the technique and confirmed that a cell could
be held throughout the acquisition of the directional and frequency data
before, during and following tipping. As described in Materials and methods,
the limitations of the tipping technique were revealed when tipping the
ipsilateral saccular otolith failed to cause a change in the DRP of a DON
unit. These data were interpreted as indicating that tipping may not always
affect the region of the saccular epithelium that provided input to the unit
from which we were recording, as saccular input is present throughout the
dorsal DON (Edds-Walton et al.,
1999). Similarly, we concluded that lack of a change in the
directional response of a cell during contralateral tipping could not be
interpreted as a lack of contralateral input, as data resulting from
unsuccessful or inadequate tipping could not be distinguished from data
indicating a lack of binaural input. Therefore, we considered only cases in
which changes in the DRP were observed during contra tipping to assess the
potential role of contralateral input to the DON.
Bilateral auditory input to the TS has been established by a previous
physiological study in the toadfish
(Edds-Walton and Fay, 2005b).
Therefore, either ipsilateral or contralateral tipping could provide insight
into the potential role(s) of binaural convergence for directional processing.
As noted above, most of the tipping experiments in the TS were conducted with
the contralateral otolith (29/31) due to space limitations in the braincase.
As in the DON, a lack of change in the DRP of an auditory unit in the TS could
not be interpreted with regard to our research question.
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Of the 36 auditory units evaluated in the DON, seven DON cells exhibited changes that were inconsistent, and nine DON cells exhibited no change in the DRP during contralateral tipping. Of the 23 auditory units evaluated in the TS, three TS cells exhibited changes that were inconsistent at different stimulus levels, and only one cell exhibited no change in the DRP during contralateral tipping.
The most common result of tipping was a change in spike rate without a shift in the shape or best direction of the DRP (47% of TS cells; 37% of DON cells). In both the TS and the DON, an increase in spike rate was slightly more common than a decrease in spike rate (Fig. 5). Total loss of activity (no spikes during tipping, with recovery post-tipping) was more common in the DON (37%) than in the TS (5%; Fig. 5). Shifts in the shape of the DRP or the best axis (in one or both planes) were always accompanied by an increase or decrease in spike rate in both the TS and the DON. At both sites, shifts in the DRP were most often accompanied by a decrease in spike rate (Fig. 5). Overall, alterations in the shape of the DRP or best axis were more common in the TS (48% of cases) than in the DON (26%).
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Contra tipping often caused an overall change in responsiveness with little or no shift in the shape of the DRP. Three DON units that exhibited rate changes are presented in Fig. 7. G4 exhibited an increase in spike activity (tipping data shown with symbols). L14 exhibited a decrease in responsiveness and a slight shift in the DRP (tipping data shown with symbols). Among DON cells, the most common result of contralateral tipping was complete loss of activity (Fig. 5). The pre-tip (larger DRP) and post-tip data (smaller DRP) are presented for cell D5 (Fig. 7) because there were no spikes produced during tipping. The smaller post-tip DRP and frequency response indicate that the unit had not recovered pre-tip activity, but the data indicate that the unit had not been lost.
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DRPs in the TS
A dramatic effect of contra tipping is shown for TS unit H1 in
Fig. 8. During tipping the
response increased in the horizontal plane, and rotation of the best axis is
present in both planes compared with the pre-tip data. The shift in the DRP is
nearly 30 deg. in each plane, and there is an interesting loss of sharpening
shown at the higher level in the mid-sagittal plane. Withdrawal of the tipping
probe resulted in a return to the original best axis in both planes. The
frequency response data are difficult to compare due to the low spike count.
The stimulus axis consistently used for the frequency stimuli was near the
null for that cell; recovery was not complete, and the spike rate was too low
for a valid frequency response post-tip at the lower of the two stimulus
levels.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Edds-Walton and Fay,
2005a). These experiments reveal some clues as to the nature of
directional computations that occur due to binaural convergence in the DON and
the TS.
Otolith tipping resulted in four responses in DON cells, presented here in
the order of their likelihood: (1) loss of activity, (2) increase in spike
rate without DRP shift, (3) decrease in spike rate without DRP shift, and (4)
a shift in the DRP shape/best axis. Given that we documented both increases
and decreases in spike rate (with or without shifts in the DRP) during
contralateral tipping, contralateral projections must include both inhibitory
and excitatory inputs. The prevalence of loss of activity in the DON during
contralateral tipping indicates that contralateral excitation is required for
at least a subset of DON cells to reach threshold, further suggesting that the
relative activity of the left and right ears
(Fig. 1A) may be compared
within the DON. Sand (Sand,
1974) illustrated that the left and right ears of the perch
respond with different directional response functions when stimulated by
particle motion in the horizontal plane, and he suggested that the combination
of right and left saccule would provide complementary directional information
with regard to azimuth of a sound source. The binaural data from the toadfish
DON are consistent with that hypothesis. The toadfish data are also consistent
with the results of the study by Horner and coleagues
(Horner et al., 1980) in cod.
They recorded reductions in the activity of auditory cells in the medulla (no
site was labeled) with ipsilateral or contralateral blocks of the eighth nerve
(Horner et al., 1980). In
addition, they were able to inhibit activity completely with a bilateral
block. Although we did not attempt bilateral tipping due to space limitations
for the tippers and the recording electrode in the skull, we expect that the
same result might be obtained with DON cells using the tipping method.
Edds-Walton presented anatomical evidence for a homotopic commissural tract
linking the dorsal auditory division of the DONs of toadfish
(Edds-Walton, 1998). The
ventral vestibular division of the DON
(Highstein et al., 1992;
Mensinger et al., 1997) also
contributes homotopic projections to the commissural tract, leading to
speculation that the commissural tract may be part of a common mode rejection
circuit, as has been described in the electrosensory medulla of skates
(New and Bodznick, 1990;
Bodznick et al., 1999). Rejection of redundant bilateral information (or
self-generated noise from opercular movements) may be a component of the DON
commissural tract, but comparison of left and right auditory inputs by
toadfish has an obvious role in directional hearing as well
(Fay, 2005).
Contralateral tipping altered the DRP of an auditory cell more often in the
TS than in the DON; however, auditory cells in the midbrain rarely lost
activity during tipping. Both findings are important for modeling the
directional circuit in teleosts. Spike rates among cells in the TS increased
or decreased during tipping, indicating that inhibition or excitation can be
associated with contralateral inputs. The persistence of some activity during
tipping (and lack of complete loss of activity) suggest that there may be
greater convergence of excitatory inputs in the TS than in the DON, which is
consistent with the convergence of binaural inputs from DON and secondary
octaval populations to the TS in toadfish, which has been demonstrated
anatomically (Edds-Walton and Fay,
2005b). Finally, shifts in the best axis for the DRP in one or
both planes (Figs 8 and
9) and, in some cases, a
broadening of the directional response (i.e. loss of sharpening;
Fig. 8) further support a role
for binaural convergence in directional computations.
Encoding the axis of particle motion of a sound source is clearly a major
driving force for the organization of the auditory pathway in toadfish and
probably other teleost fishes. Evidence from taxonomically diverse species
confirm that auditory hair cells are organized on auditory endorgan(s) along a
variety of axes, providing wide-ranging directional sensitivity. Species with
adaptations to respond to the pressure component of sound (e.g. air-filled
structures connected mechanically to the ear) are scattered throughout the
many families of fishes (Braun and Grande,
2008), but the endorgans in the ear of the pressure-sensitive
species retain particle motion sensitivity as well. Although pressure
reception is potentially important for phase comparisons that could clarify
source direction (reviewed by Fay,
2005), our work addresses the directional vector inherent in
particle motion that is encoded by the ears of all jawed fishes, including the
more ancient lineages (sturgeons) (Meyer
et al., 2005). The neural circuitry and computations associated
with the detection of particle motion in primitive fishes served as the
template for directional circuitry in modern fishes and, possibly, some
terrestrial vertebrates (Carr and
Edds-Walton, 2008).
The terrestrial tetrapod ear responds to the pressure component of sound in
air, and the auditory response from the two ears is compared in the central
nervous system, ultimately providing interaural data to `compute' the location
of the sound source [e.g. amphibians (Feng
and Shofner, 1981;
Christensen-Dalsgaard, 2005);
birds (Klump, 2000); mammals
(Brown and May, 2005)]. The
first site of binaural comparisons along the auditory pathway for most
terrestrial vertebrates is a second-order nucleus in the medulla (e.g. the
superior olive) (reviewed by Carr and
Edds-Walton, 2008). Frogs provide an interesting variation,
however. The auditory endorgans of the anuran ear project ipsilaterally to the
dorsal medullary nucleus (DMN), which projects bilaterally to a secondary
auditory nucleus (called the superior olive). There also is a commissural
tract connecting the two DMNs (Feng,
1986). Feng and Capranica
(Feng and Capranica, 1976)
provided early evidence of binaural cells in the DMN and suggested that
contralateral input could be either excitatory or inhibitory. A study by
Christensen-Dalsgaard and Kanneworf
(Christensen-Dalsgaard and Kanneworf,
2005) revealed directional sharpening in the DMN, which they
suggested was the result of binaural interactions.
Our data indicate that despite major differences in the auditory periphery,
the auditory medulla in toadfish and frogs may be organized similarly with
regard to binaural sites, although there are probably differences in the
details of the computations that occur there. Anurans have a tonotopic
organization to the DMN, and there is good evidence that both ILD and ITD are
reflected in the response properties of some DMN cells (for reviews, see
Feng and Schellart, 1999;
Christensen-Dalsgaard, 2005).
There are no comparable physiological data from a teleost fish.
To date, no well-defined vector map of auditory space has been found in
toadfish (Edds-Walton and Fay,
1998). For example, vertical tracks in the dorsal DON sometimes
yield cells with similar characteristics, but not consistently (P.L.E.-W. and
R.R.F., unpublished data). Furthermore, no study has been able to reveal a
division of the auditory circuit with response characteristics relevant to the
resolution of the 180 deg. confusion inherent in the particle motion component
of sound (Fay, 2005;
Wubbels and Schellart, 1998b).
Spatial patterns of activity, as described for directional mechanoreceptor
maps in crickets (Jacobs,
1995) is another organizational framework worthy of consideration
for the DON and TS in fishes.
Taken together, the data from the dorsal DON and the auditory TS indicate
that there are inhibitory and excitatory inputs with bilateral origins that
are combined in unpredictable ways, resulting in a variety of directional
responses. Principles proposed by Huggins and Licklider [page 299
(Huggins and Licklider, 1951)]
seem especially applicable here:
"The principle of sloppy workmanship states that it is dangerous to postulate a neural structure that is precisely arranged in detail...One of the basic facts of neurophysiology is that the nervous system works despite a considerable amount of misarrangement of detail...The principle of diversity states that the nervous system often hedges: Instead of presenting a single transform of the peripheral stimulation to the higher centers, the auditory tract may present a number of transforms...The principle of diversity suggests that a simple description of the auditory process may not be possible because the process may not be simple."
The variety of results that we obtained suggests that the circuit is not as
simple as originally modeled (Fay and
Edds-Walton, 1999; Edds-Walton
and Fay, 2003).
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