1Virginia Merrill Bloedel Hearing Research Center, 2Program in Neurobiology and Behavior, and 3Regional Primate Research Center, University of Washington, Seattle, Washington 98195
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ABSTRACT |
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Goode, Christopher T., Donna L. Maney, Edwin W Rubel, and Albert F. Fuchs. Visual Influences on the Development and Recovery of the Vestibuloocular Reflex in the Chicken. J. Neurophysiol. 85: 1119-1128, 2001. Whenever the head turns, the vestibuloocular reflex (VOR) produces compensatory eye movements to help stabilize the image of the visual world on the retina. Uncompensated slip of the visual world across the retina results in a gradual change in VOR gain to minimize the image motion. VOR gain changes naturally during normal development and during recovery from neuronal damage. We ask here whether visual slip is necessary for the development of the chicken VOR (as in other species) and whether it is required for the recovery of the VOR after hair cell loss and regeneration. In the first experiment, chickens were reared under stroboscopic illumination, which eliminated visual slip. The horizontal and vertical VORs (h- and vVORs) were measured at different ages and compared with those of chickens reared in normal light. Strobe-rearing prevented the normal development of both h- and vVORs. After 8 wk of strobe-rearing, 3 days of exposure to normal light caused the VORs to recover partially but not to normal values. In the second experiment, 1-wk-old chicks were treated with streptomycin, which destroys most vestibular hair cells and reduces hVOR gain to zero. In birds, vestibular hair cells regenerate so that after 8 wk in normal illumination they appear normal and hVOR gain returns to values that are normal for birds of that age. The treated birds in this study recovered in either normal or stroboscopic illumination. Their hVOR and vVOR and vestibulocollic reflexes (VCR) were measured and compared with those of untreated, age-matched controls at 8 wk posthatch, when hair cell regeneration is known to be complete. As in previous studies, the gain of the VOR decreased immediately to zero after streptomycin treatment. After 8 wk of recovery under normal light, the hVOR was normal, but vVOR gain was less than normal. After 8 wk of recovery under stroboscopic illumination, hVOR gain was less than normal at all frequencies. VCR recovery was not affected by the strobe environment. When streptomycin-treated, strobe-recovered birds were then placed in normal light for 2 days, hVOR gain returned to normal. Taken together, the results of these experiments suggest that continuous visual feedback can adjust VOR gain. In the absence of appropriate visual stimuli, however, there is a default VOR gain and phase to which birds recover or revert, regardless of age. Thus an 8-wk-old chicken raised in a strobe environment from hatch would have the same gain as a streptomycin-treated chicken that recovers in a strobe environment.
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INTRODUCTION |
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The vestibuloocular reflex (VOR) helps to maintain a stable image of the visual world on the retina during head movements by providing opposite movement of the eyes. The VOR is aided by the optokinetic response (OKR), which produces eye movements in the direction of the image motion that remains after the VOR. When these reflexes operating together do not produce a perfectly compensatory eye movement, visual images slip across the retina and cause the visual scene to blur. However, several lines of research indicate that the gain of the adult VOR changes in response to visual slip, thus minimizing the blur. This ability to respond to changing visual conditions produces an appropriate VOR, maintains it throughout life, and, if necessary, reestablishes the VOR after damage.
That visual slip helps maintain the VOR is well established. Adaptation
to extreme visual environments has been demonstrated in numerous
experiments in a variety of species by fitting subjects with
magnifying, minimizing, or reversing goggles to create profound retinal
slip. In response to these altered visual environments, the VOR gain
(eye velocity/head velocity) will increase, decrease, or even reverse
its sign (Gonshor and Melvill Jones 1971, 1976
;
Melvill Jones and Davies 1979
; Miles and Eighmy
1980
).
The importance of retinal slip during VOR development also has been
confirmed in numerous species. The VOR gains of dark-reared cats,
rabbits, fish, and tadpoles are lower than normal adult values
(Collewijn 1977; Harris and Cynader 1981
;
Horn et al. 1996
). Strobe-rearing, i.e., rearing an
animal exclusively in a flashing visual environment to eliminate
smoothly moving visual stimuli, and thus visual slip, also leads to
decreased VOR gain in cats (Kennedy et al. 1982
, but see
Mandl et al. 1981
). We wondered whether visual slip is
necessary for the development of the avian VOR and, moreover, whether
the slip must be experienced during a "critical period" for the VOR
to be established at all.
We tested this by rearing chicks in a stroboscopic environment from hatch and measuring the VOR at several different ages. We compared the VOR of these birds to those of normal light-reared, age-matched controls. These data provided a "time line" of the effects of strobe-rearing that, to the best of our knowledge, is not available for this or any other species.
Visual slip also may play a role during recovery from injury. In birds,
vestibular and auditory hair cells regenerate after they have been
destroyed by ototoxic, aminoglycoside antibiotics (Cruz et al.
1987; Lippe et al. 1991
; Weisleder and
Rubel 1993
). Administration of streptomycin to birds causes
most vestibular hair cells to degenerate. Within ~8-10 wk, however,
the vestibular epithelia recover their normal morphological appearances
(Weisleder and Rubel 1993
). Regenerated vestibular hair
cells apparently establish normal afferent connections because
brain-stem-evoked potentials in response to linear acceleration
resemble potentials recorded in normal controls (Jones and
Nelson 1992
).
We have shown elsewhere that horizontal VOR (hVOR) gain in the chicken
diminishes essentially to zero in response to streptomycin-induced loss
of hair cells but recovers as hair cells regenerate (Carey et
al. 1996). The vestibulocollic reflex (VCR), which stabilizes the head in space during body rotations, also recovers with hair cell
regeneration (Goode et al. 1999
). In these two studies,
chickens recovered in normal room light. It is possible that VOR and
VCR recovery from hair cell loss did not require a visual error signal and that the requisite connections to reestablish these reflexes were
guided by nonvisual mechanisms.
To test whether visual slip was necessary for VOR and VCR recovery, we treated hatchling chicks with streptomycin, allowed them to recover under stroboscopic conditions until hair cell regeneration was complete, and compared their VORs and VCRs with those of normal light-reared chickens (both streptomycin-treated and untreated, age-matched controls).
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METHODS |
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General methods
EXPERIMENTAL ANIMALS. We used white leghorn chicks (Gallus domesticus) varying in age from 2 to 40 days posthatch (dph). Strobe-reared and -recovering chickens were housed in a room lit solely by two synchronized strobe lights (American DJ), flashing at 2.25 Hz, controlled by a Grass 1000 stimulator (Grass Instruments). The stimulator was controlled by a timer, which allowed 16 h of stroboscopic light and 8 h of darkness per day (16L:8D). Chickens housed under normal light were on the same light/dark schedule.
Chickens in both the normal light and strobe conditions had unrestricted access to food and water 24 h/d. All strobe-reared chickens ate and drank normally and weighed essentially the same as normal light-reared chickens. Animal care and experimental procedures conformed to the standards of the Institutional Animal Care and Use Committee at the University of Washington.EYE COIL ATTACHMENT.
The VOR was measured with the use of Robinson's (1963)
magnetic search coil technique. Prefabricated eye coils, whose leads were twisted together and soldered to small, gold, female connector pins (Amphenol) that were imbedded in a small plug of dental acrylic, were implanted on the sclera (see Anastasio and Correia
1988
; Quinn et al. 1998
) of the left eye of each
bird 48 h before testing (except for 2-day-old chicks, which
received the eye coil 1 dph). Surgical procedures were performed with
the birds under equithesin and ketamine anesthesia (1.5 ml/kg; 0.8 mg/kg, respectively). Strobe-reared chickens were
anesthetized under strobe light and were returned to the stroboscopic
environment for surgical recovery.
VOR TESTING. Both the horizontal (yaw, about a vertical axis) and vertical (roll, about the anterior-posterior axis) VOR were measured in all chickens. All VOR testing was done in the dark. All strobe-reared chickens were prepared for testing in a darkened room.
Alert chickens were restrained in a supine plastic bottle with a hole cut out for the head. The heads of the birds were restrained by taping the beak firmly to a bone wax-lined beak holder, which was attached to the bottle, extending from the hole cut for the head. The bottle was then secured to a rotating turntable. The turntable was set to oscillate over a fixed angle of ±10° at frequencies of 0.1, 0.3, 0.5, and 0.8 Hz, i.e., at peak velocities of 6.28, 18.85, 31.42, and 50.2°/s, respectively. Two pairs of 14-in magnetic induction coils that produced alternating magnetic fields (35 kHz) at the subject's left eye rode on the turntable. Horizontal and vertical angular eye position signals were filtered at 500 Hz and recorded on video tape (Vetter 5000A PCM recorder, sample rate = 5 kHz/channel). Turntable position was measured with a potentiometer. All signals were simultaneously digitized on-line with a Power Macintosh 7500/120 MHz and a MIO16 Digitizer (National Instruments). Digitizing software set the sampling rate at 600 samples for every cycle of oscillation, regardless of the frequency. Search coils were calibrated at the beginning of each test session by suspending the animal in the center of the electromagnetic field and oscillating the turntable (and coils) at a frequency of 0.3 Hz around the animal, whose eyes remained essentially stationary in space.VOR DATA ANALYSIS AND VECTOR AVERAGING. An interactive analysis program displayed single cycles of digitized sinusoidal horizontal or vertical turntable position, along with horizontal and vertical eye position, on a computer monitor. The program calculated digital derivatives of all position traces to produce velocities and fit each trace with a best-fit sine wave using a discrete Fourier transform (Fig. 1, top 3 traces). The rapid, nonperiodic saccades were easily identified by their rapid oscillations (see horizontal eye velocity) and were removed (Fig. 1, bottom traces). The program then calculated VOR gain for each cycle of the saccade-free data as the ratio of eye to turntable velocity and the phase shift as the difference (in degrees) between the peak of the fitted turntable (and therefore head) velocity sinusoid and the peak of either the horizontal or vertical eye velocity sinusoid. By our convention, a perfectly compensatory VOR has a gain of 1.0 and a phase shift of 180°. Phase shifts between 0 and 180° indicate that eye velocity led head velocity.
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EXPERIMENT 1: EXPERIMENTAL DESIGN AND EXPERIMENTAL ANIMALS. The independent variables were age (4 levels) and lighting condition (stroboscopic and normal), yielding eight groups. Subjects were randomly assigned to these groups as follows. Of 56 chickens, 28 were placed in an incubator in the strobe environment 2 days before they hatched. After hatching, chicks were moved to brooders in the same stroboscopically illuminated room. Reptile heating pads (Cobra) on the floors of the brooders provided heat without light. The other 28 chicks were hatched in a normally illuminated (16L: 8D) incubator and served as age-matched controls. The horizontal and vertical VOR (hVOR and vVOR) were measured in strobe- and normal light-reared birds in four age groups: 2, 9, 25, and 40 dph (n = 7 at each age). Immediately after VOR testing, the strobe-reared, 40-dph chickens were moved to normal light conditions for 3 days and then tested again.
EXPERIMENT 2: EXPERIMENTAL DESIGN, EXPERIMENTAL ANIMALS AND
STREPTOMYCIN TREATMENT.
The independent variables were streptomycin treatment (treated and
untreated) and lighting condition (stroboscopic and normal). Chickens
were randomly assigned to one of the resulting four groups (n = 4 in each group) as follows. Of 24 white leghorn
chicks, each 7 dph, 12 were injected with streptomycin sulfate (1,200 mg · kg1 · d
1 im, for 5 days). This treatment produces
profound damage of vestibular hair cells and reduces the gains of the
hVOR and vestibulocollic reflex (VCR) to zero (Carey et al.
1996
; Goode et al. 1999
). The h- and vVOR of
four streptomycin-treated birds were measured 2 days after the last
injection and compared with those of four untreated, age-matched controls.
STATISTICAL ANALYSES. Repeated-measures analyses of variance (ANOVA, Statview 4.5) were used to compare mean vector-averaged gain and phase data from strobe-reared and normal light-reared birds in both experiments. In experiment 1, between-subjects variables were age (4 levels) and lighting condition (stroboscopic vs. normal). In experiment 2, between-subjects variables were streptomycin treatment (treatment vs. no treatment) and lighting condition (stroboscopic vs. normal).
Scheffe post hoc tests (Statview 4.5) were used to compare means where significant main effects or interactions were detected by the ANOVA. Where ANOVA statistics are reported, the values of F and P (probability) are presented and between- and within-subjects degrees of freedom, respectively, are given in parentheses. Whenever individual means were compared, the probability value presented is the result of a Scheffe post hoc test. We consider probabilities <0.05 to be significant for both ANOVA and Scheffe statistics.VCR TESTING.
The VCR was measured in five additional chickens, of which three
received the same dose of streptomycin as the 7-day-old chicks described in the previous section. All five chicks were placed in the
stroboscopic environment the day after the streptomycin-treated chicks
received their last injection. The VCR in these birds was measured
after 21 days of recovery in the stroboscopic environment by which time
VCR recovery under normal light is known to be complete (Goode
et al. 1999). The head movements of the VCR were measured via a
search coil attached to the side of the chicken's head (for measurement and analysis details, see Goode et al.
1999
).
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RESULTS |
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Experiment 1
VOR DEVELOPMENT IN NORMAL LIGHT-REARED CHICKENS. Gain. Average h- and vVOR gains were low (between 0.15 and 0.4 depending on frequency) when they were first measured at 2 dph (Fig. 2). Generally, both h- and vVOR gain increased with frequency [F(3, 48) = 290.15, P < 0.0001; F(3, 48) = 155.68, P < 0.0001, respectively] until 0.5 Hz, after which gain appeared to saturate (Fig. 2). Since the oscillation was of fixed amplitude, however, gain could have been related to velocity rather than frequency.
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VOR DEVELOPMENT IN STROBE-REARED CHICKENS.
In normal chickens, significant differences in VOR gain and phase
shift occur between the lowest and highest stimulus frequencies (Carey et al. 1996). The lowest frequencies have the
lower gains and the greater phase leads. We therefore compared the h-
and vVOR of strobe-reared chickens with those of normal-light-reared chickens at the lowest and highest oscillation frequencies.
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EFFECTS OF PLACING STROBE-REARED CHICKENS IN NORMAL LIGHT. Immediately after strobe-reared chickens were tested 40 dph, they were moved to normal light conditions (16 h continuous light, 8 h dark). After 3 days of exposure to ambient room light, the hVOR gain in strobe-reared birds had increased at 0.1, 0.3, and 0.5 Hz (Fig. 6A). However, h- and vVOR gains in these chickens were still significantly lower overall than those of normal-light-reared chickens at all frequencies except for the vVOR at 0.8 Hz (Fig. 6, A and C; hVOR: 0.1 Hz, P < 0.01; 0.3 Hz, P < 0.005; 0.5 Hz, P < 0.01; 0.8 Hz, P < 0.05; Fig. 6C: vVOR: 0.1, 0.3, 0.5 Hz, P < 0.05; 0.8 Hz, P > 0.5).
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Experiment 2
VOR RECOVERY OF STREPTOMYCIN-TREATED CHICKENS UNDER NORMAL LIGHT. One day after streptomycin treatment, both h- and vVOR gain were reduced essentially to zero at all frequencies (Fig. 7, A and B). The actual gains are shown in Fig. 7 to confirm that they all are <0.1, our inclusion threshold.
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VOR RECOVERY OF STREPTOMYCIN-TREATED CHICKENS IN A STROBOSCOPIC ENVIRONMENT. Allowing streptomycin-treated birds to recover in a stroboscopic environment prevented hVOR gain from recovering to normal values at all frequencies <0.8 Hz. Chickens that recovered in the stroboscopic environment had significantly lower hVOR gains at 0.1, 0.3, and 0.5 Hz than chickens that recovered in normal light (P < 0.001; P < 0.001, and P < 0.01, respectively). In fact, the hVOR gains of all strobe-recovered birds were lower than those of birds housed in normal light, whether they had been treated with streptomycin or not [Fig. 9A; F(1, 12) = 23.05, P < 0.005].
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VOR IN STROBE-RECOVERED CHICKENS AFTER 48 H OF NORMAL LIGHT. Streptomycin-treated, strobe-recovered chickens were placed in normal light immediately after VOR testing 8 wk after streptomycin treatment. They were tested again ~48 h later at 0.1, 0.3, and 0.5 Hz. At this age, the chickens were quite large and boisterous, preventing measurement at the highest frequency of oscillation. Exposure to normal light brought the hVOR back to normal at all frequencies. Horizontal VOR gains in streptomycin-treated, strobe-recovered chickens that were exposed to normal light for 48 h were not significantly different from those of untreated chickens that were housed in normal light [Fig. 10A; F(1, 6) = 0.11, P > 0.5].
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VCR RECOVERY OF STREPTOMYCIN-TREATED CHICKENS IN A STROBOSCOPIC
ENVIRONMENT.
Three additional chicks were treated with the same dose of streptomycin
(1,200 mg · kg 1 · d
1 for 5 days) and allowed to recover in
the stroboscopic environment along with two additional untreated chicks
that were used as controls. After 3 wk, by which time the VCR recovers
fully under normal light (Goode et al. 1999
), the VCR
was measured in all chickens and compared with that of untreated
chickens housed in normal light in a previous experiment (Goode
et al. 1999
).
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DISCUSSION |
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Chickens that were reared from hatch in a stroboscopic environment, which eliminates visual slip, failed to develop a normal VOR. Both the gain and phase shifts of the VOR remained immature through 40 dph. Chicks that were treated with streptomycin at 7 dph and then placed in a strobe environment did not recover their VOR although streptomycin-treated chicks that recovered in normal light did. The VOR gain and phase shifts of streptomycin-treated, strobe-recovered chickens were similar to the gain and phase shifts of strobe-reared chickens of a similar age. Together, these experiments show that for a change in the VOR to occur, chickens must experience visual slip. This is true whether that change is over the course of development or during recovery from hair cell loss. In the absence of visual slip, the VOR has abnormal characteristics, which are the same in both streptomycin-treated and untreated birds. However, when slip is restored even after a long period of 40 days, the VOR still can improve.
Poor image stabilization early in development
Our results are consistent with other reports that the gain of the
hVOR in newly hatched chickens is low, ranging from ~0.07 at 0.125 Hz
to ~0.2 at 1.0 Hz (Carey et al. 1996; Wallman
et al. 1982
). By 4-6 wk of age in normal ambient light, hVOR
gain increases to 0.35 at 0.125 Hz and to 0.6 at 1.0 Hz (Wallman
et al. 1982
). Our measurements of hVOR gain (Fig. 2) at 40 dph
are nearly identical to those reported by Wallman et al.
(1982)
and Carey et al. (1996)
.
At low frequencies, both the gain and phase of the VOR, which is
measured in the dark, would not provide adequate image stabilization. At higher frequencies and older ages, the gain and phase become more
compensatory but far from ideal. If the adult chicken is oscillated in
the light to activate the optokinetic reflex as well as the VOR, the
gain of the compensatory eye movements is near 1.0 at all frequencies
tested (0.125-1.0 Hz) (Wallman et al. 1982).
The time course of VOR development in chickens is much longer than the
development of several other visual capabilities. For example, both
depth perception (Shinkman 1963; Tallarico and
Farrell 1964
) and visual acuity (Over and Moore
1981
) in chickens are fully developed by 2 dph. Thus
developmental changes in VOR gain and phase shift are probably not
secondary to, nor a consequence of, immature visual processes.
Different time courses of VOR gain and phase development
The gain of both the h- and the vVOR followed a different developmental time course than did their associated phase shifts. For both the vVOR and hVOR, little change in gain occurred between the 2nd and 25th dph. The greatest change occurred between the 25th and 40th day, when gain increased significantly (Fig. 2, A and B). In contrast, the phase shift of the hVOR showed very little change (<10° at each frequency) over the same 40-day period. Between 2 and 40 dph, the phase shift of the vVOR showed a slightly more substantial increase, on the order of 20° (Fig. 3, A and B).
Different time courses of the gain and phase changes also occur during
VOR adaptation with optical devices. In cats whose VOR was adapted with
reversing prism masks, hVOR gain decreased rapidly in the first 10 days, but hVOR phase shifts did not change noticeably until after 10 days. When the prisms were removed, the phase shift returned to
preadapted levels within the first few days, but it was much longer
before the gain approached its preadapted state (Melvill Jones
and Davies 1979). VOR gain and phase, then, can be adapted at
different rates when the visual environment is artificially controlled.
Our study shows that VOR gain and phase shift develop at different
rates as well, suggesting that gain and phase can be adjusted
independently in a variety of situations.
Development of the VOR in a strobe environment
Chickens reared from hatch in the strobe environment did not develop a normal VOR. Strobe-rearing affected both the h- and vVOR at all frequencies of oscillation but especially at lower frequencies. The gain of the VOR at 0.1 Hz was near zero in strobe-reared chickens at each age tested (Fig. 4). These low gains prevented us from measuring phase shifts reliably. Generally, the effects of strobe-rearing were not as robust at 0.8 Hz, although VOR gains were still significantly lower in strobe-reared chickens on most test days (Fig. 5, A and C). At this frequency, h- and vVOR phase shifts did not develop, i.e., they remained unchanged for the entire 40 days of the experiment (Fig. 5, B and D).
The frequency dependence of the effects of strobe-rearing suggests a
symbiosis with the frequency characteristics of the developing optokinetic response (OKR). At 0.1 Hz, the OKR has a higher gain than
the VOR in both young and older chickens (Wallman et al. 1982) and thus contributes more to compensatory eye movements in a visual environment at this frequency. At 0.8 Hz, OKR gain is <0.1
in adult chickens (Wallman et al. 1982
) and therefore contributes little to compensatory eye movements. Therefore depriving chickens of smoothly moving visual input affects the VOR more at
frequencies where visual following generated by the OKR would normally
aid gaze stabilization.
The effects of altered visual environments, either strobe- or
dark-rearing, on both the h- and the vVOR have been examined in several
other species. Dark-rearing until either 3 or 7 mo of age in rabbits
(Collewijn 1977; Favilla et al. 1984a
,b
)
or for 11-15 mo of age in cats (Harris and Cynader
1981
) reduced VOR gain by about half, on average, although
phase shifts were close to normal. Similarly, strobe-reared cats had a
significantly lower VOR gain after 14 mo of strobe-rearing
(Kennedy et al. 1982
). In congenitally blind adult
humans, the VOR is completely absent (Kömpf and Piper
1987
; Sherman and Keller 1986
). Those studies showed that a normal visual environment is necessary for the
development of the VOR. Here, we show that deprivation of visual slip
has both immediate and late effects on VOR development. Horizontal VOR
gain in strobe-reared chicks was significantly lower than that of
normal-light-reared chicks after only 2 days in the strobe environment
(Figs. 4A and 5A). On the other hand, the effects of strobe-rearing on the VOR phase shift were not apparent until 25-40
dph (Fig. 5, B and D).
Rescue of the strobe-reared VOR gain by brief exposure to continuous light
After strobe-rearing, exposure to normal light for 3 days drove
both the gain and phase shift of the VOR toward normal values. However,
the gains of both the h- and vVOR in these chickens were still
significantly lower than in normal-light-reared chickens (Fig. 6,
A and C) although the difference was less for the
vVOR. In contrast, the phase shift of the v- and hVORs essentially
recovered completely. These data provide additional support for our
earlier suggestion that the gain and phase (direction) of the VOR can be adjusted somewhat independently. Because the hVOR phase of cats
fitted with reversing prisms returns to normal more rapidly than does
hVOR gain (<5 vs. >30 days) (Melvill Jones and Davies 1979), we may have missed subsequent VOR gain changes by
leaving our strobe-reared birds in normal light for only 3 days.
Some recovery of VOR function by exposure to normal light after dark-
or strobe-rearing has been demonstrated in mammals. Dark-reared rabbits
recover some (Collewijn 1977) or all (Favilla et
al. 1984a
) VOR function after normal light exposure. However, dark-reared (Harris and Cynader 1981
) and strobe-reared
(Kennedy et al. 1982
) cats fail to develop a normal VOR
even after 5 mo in normal light. This suggests that cats have some
critical period when visual slip is crucial for VOR development.
Our results suggest that if there is a critical period for normal VOR development in the chicken, there may be different critical periods for gain and phase. Since VOR phase recovered completely after 40-dph strobe-reared chickens were exposed to normal light for only a few days, the critical period for VOR phase must extend past 40 days, if one exists at all. Since VOR gain in these birds showed some improvement, but was still significantly lower than in normal-light-reared chickens, the critical period for VOR gain may be close to 40 days.
Recovery from streptomycin treatment
As shown in our previous studies, streptomycin effectively eliminates the hVOR immediately after treatment. We show here that the vVOR is similarly compromised. After 8 wk of recovery under normal light, the hVOR recovered completely (Fig. 8, A and B) but the vVOR gain was still significantly lower than that of untreated controls (Fig. 8, C and D).
What could account for the differential recovery of the h- and vVOR? One possibility is that there isn't sufficient vertical slip to drive vVOR adaptation. If, during recovery, a chicken experienced less slip in the vertical plane than in the horizontal, one might expect to see more recovery in the hVOR than the vVOR. However, chickens that were recovering in normal light made numerous head movements about the roll axis, apparently to direct gaze toward the floor of their cage where the feed was scattered. These head movements would create vertical slip when the VOR gain was recovering. Therefore the difference between h- and vVOR recovery cannot be explained by insufficient visual slip in the vertical plane.
A second possibility is that there is a late recovery of the type of
hair cell that may be primarily responsible for the vVOR. After 8 wk of
recovery, hair cell regeneration is largely complete, but the density
of Type I hair cells still is lower in streptomycin-treated chickens
than in age-matched controls (Carey et al. 1996;
Goode et al. 1999
). These differences are not
significant, but it is possible that the vVOR is more dependent on Type
I hair cells than is the hVOR. Although this explanation is much more
likely than insufficient vertical visual slip, we do not have enough information to accept it conclusively. If it is true, future studies should find that the density of Type I hair cells is correlated more
strongly with vVOR gain than with hVOR gain and that the vVOR should be
fully recovered when the regeneration of Type I hair cells is complete.
Effects of strobe illumination on hVOR recovery
The major finding of experiment 2 is that visual slip
is necessary for the complete recovery of the hVOR after streptomycin treatment. Both the gain and phase shift of the hVOR were generally lower than normal in strobe-recovered chickens whether they were treated with streptomycin or not (Fig. 9). These data suggest that
functional recovery from hair cell damage cannot be explained solely on
the basis of neuronal factors such as axon guidance or the ratio of
different hair cell types. In retrospect, this is perhaps not so
surprising. Complete functional recovery after hair cell damage depends
on several events. Hair cells must regenerate and differentiate into
either Type I or II (Weisleder et al. 1995). The
regenerated hair cells then must make afferent connections with the
appropriate fibers of the 8th nerve. These connections must be very
specific: Type I hair cells generally should connect with regularly
firing afferents and Type II hair cells with irregularly firing
afferents. In turn, these afferents must be connected to circuits
involved in either the hVOR, vVOR, or VCR. We show here that this
complicated process is facilitated by visual slip signals.
Rescue of hVOR gain by normal light
When our streptomycin-treated, strobe-recovered chickens were then
exposed to normal light for only 48 h, the gain and phase of the
hVOR recovered almost to normal (Fig. 10). This finding is in marked
contrast to results in cats and rabbits. Strobe-reared (Kennedy
et al. 1982) and dark-reared (Harris and Cynader
1981
) cats failed to recover the VOR when exposed to normal
light, and dark-reared rabbits had only partial recovery when
subsequently exposed to normal light (Collewijn 1977
;
Favilla et al. 1984a
,b
). Apparently, birds and mammals
have different adaptation mechanisms. A VOR adaptation mechanism is
functional early in the life of the bird. As soon as they hatch, chicks
exhibit hVOR gain changes to retinal slip stimuli (Wallman et
al. 1982
). Our results suggest that this adaptation system
remains ready to adjust hVOR gain even after 40 days of deprivation
from its relevant error signal.
Effects of strobe illumination on VCR recovery
Although we tested only a small number of animals, our preliminary
data indicate that retinal slip does not affect the VCR in the same way
as it does the VOR. At frequencies >0.3 Hz, VCR gain in
streptomycin-treated/strobe-recovered chickens was identical to that in
untreated chickens housed in normal light (Fig. 11). Furthermore these
data indicate that, as expected, the vestibular organs were not
directly affected by strobe-rearing as they still were able to drive
the VCR normally at all frequencies 0.3 Hz. In fact, at 0.1 Hz, we
detected low VCR gains in only two streptomycin-treated, strobe-recovered chickens. Therefore the effects of stroboscopic illumination on the VOR must be strictly visual in nature. These data
suggest that some other error signal must help guide recovery of the
VCR. Perhaps there is sufficiently accurate information from the neck
receptors to reestablish normal VCR gain after streptomycin damage.
General conclusions
The results of these two experiments support the hypothesis that the major factor that determines the status of an improving VOR, whether the improvement occurs during development from hatch or during recovery from hair cell loss, is the visual environment. However, some functional recovery occurs even in the stroboscopic environment. It is possible that during recovery from streptomycin intoxication, regenerating hair cells are soon contacted by the correct nearby afferent terminals, which have retained their central VOR connections. As more hair cells are produced and connect, hVOR gain increases even without proper visual feedback that the VOR is improving. The same argument could be used to explain the partial development of the VOR in the absence of visual slip.
Perhaps visual information is being used in our strobe environment but only at the fastest natural head velocities. It is possible (though unlikely) that very rapid head movements during the brief flash of the strobe create some retinal slip, which accounts for the relatively more normal hVOR behavior at high frequencies.
In any case, it appears that without any useful visual feedback, both the recovering and developing hVOR progress (or revert) to the same default gain and phase shift values regardless of age. When appropriate visual feedback is reintroduced, however, both the developing and recovering VOR still are capable of further improvement.
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ACKNOWLEDGMENTS |
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We are grateful for the editorial acumen of K. Elias. The authors gratefully acknowledge J. Phillips for expert animal care, S. Rude for surgical training, S. Brettler for suggesting the vector averaging method, and J. Debel and B. Enger for housing C. T. Goode.
This study was supported by National Institutes of Health Grants RR-00166, EY-00745, and DC-02854 and by the Virginia Merrill Bloedel Hearing Research Center.
Present address of C. T. Goode and D. L. Maney: Dept. of Psychology, Johns Hopkins University, Baltimore, MD 21218.
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FOOTNOTES |
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Address for reprint requests: A. F. Fuchs, Regional Primate Research Center, Box 357330, University of Washington, Seattle, WA 98195-7330 (E-mail: fuchs{at}u.washington.edu).
Received 25 July 2000; accepted in final form 8 December 2000.
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REFERENCES |
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