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.)
Peggy L. Edds-Walton1,* and
Richard R. Fay2
1 Parmly Hearing Institute, Loyola University Chicago, Chicago, IL 60626,
USA
2 Neuroscience Institute, Marine Biological Laboratory, Woods Hole, MA 02543,
USA
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Fig. 1. (A) Dorsal view of toadfish brainstem illustrating recording and otolith
tipping methods. The recording electrode surveyed the approximate area of the
descending octaval nucleus (DON) shown as a white oval. The tipping probe and
recording electrode are drawn to indicate approximate locations during
experimentation. The tipping probe was used to tilt the curved edge of the
saccular otolith 20–30 deg. laterally from normal orientation with
respect to the midline of the fish (contralateral tip illustrated). (B)
Cartoon of dorsal view of toadfish to illustrate location of paired saccules
(not drawn to scale). The black structures represent the otoliths, and white
structures medially represent the sensory epithelia. The right epithelium is
enlarged to illustrate the hair cell orientation pattern
(Edds-Walton and Popper,
1995 ). Arrowheads point to the best direction for hair cells in
that region; note that well-defined, opposition zones (orthogonal hair cells)
are not present on the toadfish saccule. The large curved arrow indicates the
direction of rotation during contralateral tipping. Abbreviations: Cb,
cerebellum; Ob, obex; OT, optic tectum of midbrain; sac, saccule.
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Fig. 2. Multi-unit activity illustrated prior to tipping the ipsilateral saccular
otolith (Pre), during tipping (Tip) and after otolith returned to its original
orientation (Post-tip) at three different recording sites in the DON of two
fish (M, L).
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Fig. 3. Examples of negative results from tipping the saccular otolith. Tipping of
the ipsilateral saccular otolith resulted in no change in the directional
response pattern (DRP) of unit G14 in the DON to stimuli in the horizontal or
mid-sagittal planes; tipping of the contralateral saccular otolith did not
cause a change in the DRPs of unit F1 in the torus semicircularis (TS).
Stimulus level shown in dB re: 1 nm. Note that each unit was held for
consistent data acquisition throughout the experiment and that the slight
variation in response magnitude at each direction is consistent with normal
variation in the absence of manipulation. Filled circle on curve for pre-tip
data; no symbol for data during tipping; x used for post-tip
data.
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Fig. 4. Anatomical evidence of a commissural auditory pathway connecting the DONs.
(A) Coronal section with large neurobiotin injection at physiologically
characterized auditory site (vertical arrow) in left dorsal DON. White box
indicates area enlarged in B (right-angle arrow indicates contralateral cut in
brain prior to sectioning). (B) Projection cell in DON among other filled
somata; axon (arrows) entered the commissural tract. (C) Contralateral site in
the same fish, 100 µm caudal of A, with terminal fields in the right dorsal
DON (asterisk) from projection cells in the left dorsal DON. (D) Contralateral
site in the same fish, 50 µm rostral of A with terminal fields (asterisk)
from left dorsal DON projections and retrogradely filled somata of projection
cells in the right dorsal DON (black box, enlarged in E). (E) Retrogradely
filled projection cells from D. Scale bar, 100 µm in B and E; 400 µm in
C and D; 1 mm in A. Vd, descending tract of trigeminal; ven ventricle; and
VII, sensory facial nerve.
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Fig. 5. Categories of responses to contralateral tipping of the saccular otolith in
the DON (shaded) and the TS (hatched) of the toadfish. Data are graphed as a
proportion for each site (i.e. total of 100% for DON, total of 100% for TS).
Note that all units exhibited a change in spike rate: data are divided to
illustrate the proportion of units that exhibited only spike rate changes and
those that exhibited spike rate changes along with shifts in the best axis or
altered shape of the DRP. No spikes category (No S s–1)
indicates units that lost spike activity during tipping, but resumed spike
activity following removal of the tipper; S s–1, spikes
s–1; Inc., increase; Dec., decrease. DON: N=38; TS:
N=23.
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Fig. 6. Example of DRP changes with tipping of the ipsilateral saccular otolith for
a DON unit. DRPs for both stimulus planes and frequency responses are shown
pre-tip, during tip and 5 min post-tip. Two different stimulus levels are
plotted for each DRP graph (20 and 25 dB re: 1 nm, higher level has symbols);
spike rate indicated by the circle (100 spikes s–1).
Interpolated best axes (average of two levels) pre-tip: –30 deg. (left)
azimuth, 85 deg. elevation; tipped: 35 deg. (right) azimuth, 62 deg.
elevation; post-tip: –30 deg. (left) azimuth, 80 deg. elevation.
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Fig. 7. Examples of different spike rate changes in DON units due to tipping
contralateral saccular otolith. Symbols identify data obtained during tipping,
except for D5. G4: increase in spike rate; L14: decrease in spike rate. D5:
all activity was lost during tipping; spike activity was lower post-tipping
(smaller curves) than pre-tipping (larger curves) due to incomplete recovery.
Frequency responses shown on the right. S s–1, spikes
s–1, indicated by the circular scale; stimulus levels in dB
re: 1 nm.
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Fig. 8. Experimental data set for cell H1 in the TS. DRP and frequency response are
shown pre-tip, during tip and 5 min post-tip of the contralateral saccular
otolith; higher stimulus level indicated by symbols. The higher stimulus level
had a slightly smaller DRP in both planes pre-tip. Increased spike rates and a
shift in the best axis in the DRP occurred in both planes during tip.
Interpolated best axes (average of two levels): pre-tip azimuth 60 deg.,
elevation 90 deg.; tipped azimuth 37 deg., elevation 65 deg.; post-tip azimuth
55 deg., elevation 85 deg. Stimulus levels: 20 and 25 dB re: 1 nm; circular
scale for DRP is 20 spikes s–1. Frequency responses are
minimal because the standard stimulus axis was near the null for this
unit.
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Fig. 9. Responses of four units in the TS to tipping. Circular symbols identify
tipping data. P6: altered DRP and decreased spike rate in mid-sagittal plane,
altered best axis in horizontal plane. F8: DRP altered in both planes,
increased sharpening in horizontal plane and rotation of DRP in mid-sagittal
plane. M5: change in spike rate in vertical plane only, no shift in best axis.
M1: major reduction in spike rate in both planes, little or no change in DRP.
Frequency response shown on the right. Spikes s–1, indicated
by circular scale; stimulus levels in dB re: 1 nm.
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© The Company of Biologists Ltd 2009
