EXPERIMENTAL
NEUROLOGY
115,69-72
(1992)
Recovery of Contrast Sensitivity during Optic Nerve Regeneration in Fish’ D.P.M. ~epurt~e~t
NORTHMOREAND
of ~sycko~gy and Neuroscience ~ogru~,
Psychophysical experiments on goldfish and sunfish studied the recovery time course of visual contrast detection during optic nerve regeneration. The results showed delayed recovery of detection of positive as compared to negative contrasts, and of high as compared to low spatial frequencies. The findings are related to previous electrophysiological and anatomical results in the fish retinotectal system. Q 1992 Academic Press,
Inc.
The teleost optic nerve readily regenerates after it is crushed. Behavioral tests, have tended to show virtually complete recovery of vision (7, 9), suggesting that regenerating optic nerve fibers eventually reestablish normal central connections. Anatomical studies in goldfish have shown that by about 20 days postcrush, the optic tectum contains regenerating optic axons with synapses upon tectal cells (1, 12). Many of these axons branch very extensively over the tectal surface. By about 40 days, optic terminal arbors are located at appropriate retinotopic positions over the tectal surface, with fewer arbors of large extent (2,ll). This process of refinement of the retinotectal map has also been studied electrophysiologically, mainly by recording visually evoked activity from optic nerve terminals in the superficial layers of tectum. Such recordings have found enlarged mult~unit receptive field (MURFs) that shrink to normal dimensions over time (10). Thus both anatomical and physiological approaches show that the retinotectal projections are refined by progressive shifting and reshaping of arbors. To assess the transmission of useful visual information by the regenerated retinotectal interface, we are currently using psychophysical methods to measure the contrast sensitivity of fish undergoing optic nerve regeneration. Our aims are to relate recovery to the changes in the retinotectal projection revealed anatomically and physiologically, and to see whether the various * This work Eye Institute
was supported of NIH.
by a grant
(EY02697)
from
the National
M.A.
CELENZA
Un~uers~ty of ~elu~~re,
visual information courses of recovery.
repark,
~eluware
channels
ELECTROPHYSIOLOGY:
19716
exhibit
MURF
different
time
REFINEMENT
Electrophysiological experiments in our laboratory have characterized MURFs quantitatively during optic nerve regeneration in goldfish (4, 5) using two kinds of stimuli differing primarily in the sign of their contrast. The first was an array of miniature, red light-emitting diodes (LEDs) that were flashed in the fish’s visual field; the second was a black vertical stripe (10’ wide) rotated slowly through the visual field. Both stimuli were presented against the same illuminated background at photopic levels (15 cd/m’). Figure 1 compares the widths of MURFs obtained with these two stimuli in different goldfish at various times after optic nerve crush. Using the black-stripe stimulus, visually evoked activity was first detected at about 20 days postcrush in tectum and in torus longitudinal& The latter is a nucleus with no direct retinal input that receives dimming information from tectal neurons (3). MURF widths were initially much enlarged but recovered gradually, approximated by an exponential decay with a time constant of 26 days. The LED stimuli, however, did not reliably evoke unit activity in tectum until about 40 days postcrush, although OFF responses could be observed with high-contrast stimulation. Several MURF characteristics, in addition to their widths (Fig. lB), showed that LED-sensitive MURFs, when they appeared, rapidly returned to normal. The results suggest that visual channels carrying dimming or OFF information recover first, followed by those carrying ON information. PSYCHOPHYSICS: POSITIVE AND CONTRAST SENSITIVITY
NEGATIVE
To see whether these differences in recovery time observed electrophysiolo~cally represent ~~~ctio~l reconnection of different information channels, goldfish were tested psychophysically for their ability to detect both positive and negative contrast stimuli during optic nerve regeneration. Goldfish were kept at 25°C and classically condi69
0014-4886/92
$3.00
Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
70
NORTHMORE NEGATIVE
CONTRAST
STIMULI
500 400
-
0
TECTUM
.
TL
,-_------------------~_~_ 0 ’ 0
__,
I
I
I
I
I
I
20
40
60
80
100
120
POSITIVE
CONTRAST
I 140
STIMULI
AND
CELENZA
dures were programmed for each stimulus type, such that after a hit trial, disk contrast was lowered by 0.25 log unit for the next presentation of that stimulus, otherwise it was raised by 0.25 log unit. Fish were typically tested every other day. Figure 2 compares the detection recovery of negative and positive contrast disk stimuli (1.6” diam) presented to the crushed side of one goldfish. The upper half of each figure shows suppression ratios in each trial. Values around 1.0 indicate no response to the negative disk stimuli until about 30 days for negative contrast, and 39 days for positive disks. The lower halves of each figure show how disk contrast tracked the fish’s contrast
(Ofl(mj
200 ------
~~~I~--~-~~~-------~-~~-
100 0'
L----------------------I 0 20
I 40
4 60 DAYS
I 80 POSTCRUSH
1 100
I 120
0
1 I 140
FIG. 1. Electrophysiological determinations of recovery of multiunit receptive field (MURF) dimensions in the goldfish visual system after crushing one optic nerve. The half-maximum widths of MURFs recorded from tectum or torus longitudinalis (TL) are shown as a percentage of control values. Horizontal dashed lines show f2 standard deviations. Upper: Activity was evoked by a 10’ wide vertical black stripe moving slowly through the visual field. Each data point is the mean of several MURFs recorded from one fish. Lower: Stimuli were flashed red LEDs. Data are from individual receptive fields yielding multiunit activity that was statistically discriminable from background activity.
tioned to visual stimuli using respiration suppression as the conditioned response (6). Fish were restrained in a holder such that one eye faced a video display screen (23 x 20 ems) at an apparent underwater distance of 44 ems. A motor rotated the fish holder to allow testing of either eye. A thermistor in front of the mouth was used to monitor respiration amplitude and frequency. Between trials, the display screen showed a neutrally colored, uniform background of 30 cd/m2; during a trial, one of four types of stimulus disk, 1.6 or 16” diam of either positive or negative contrast, was presented in the screen center for 5 s. Suppression of respiration was conditioned by pairing the offset of the stimulus disk (log contrast = -0.25) with mild electric shock to the tail. After training fish to a criterion using left and right eyes in alternation, one optic nerve was crushed intraorbitally. A computer presented the different stimuli in random order, rotated the fish to test the crushed or uncrushed side, and scored a hit if respiration amplitude was suppressed by more than 50%. In order to track contrast thresholds over time, separate staircase proce-
0
10
20
30
40
50
50
70
80
90
1 K)
6 1.53
I
0
10
20
30
40
50
60
70
80
so
loo
DAYS POSTCRUSH FIG. 2. Psychophysical determination of the time course of recovery of contrast detection in one goldfish using its regenerating optic nerve. Stimuli were 1.6” disks, either negative contrast (A) or positive contrast (B). The upper halves of each figure show respiration suppression ratios calculated as the mean respiration amplitude during the stimulus presentation, divided by the mean amplitude over 15 s before stimulus presentation. A value of 1.0 indicates no suppression response; 0.0, full suppression response. Lower halves show trial-by-trial stimulus contrast tracked by a staircase procedure. The continuous horizontal lines show the mean contrast threshold of the control eye obtained at the same time.
VISUAL
CONTRAST
RECOVERY
IN
71
FISH
Low Spatial Frequency (0.15 c/deg)
threshold. For both negative and positive disks, threshold followed a downward trend, reaching control levels only after about 70 days postcrush. Similar trends were also found for the large (16”) disks. In five other goldfish tested so far, negative contrasts were detected about 10 days before positive contrasts.
---
2l--
PSYCHOPHYSICS: CONTRAST SENSITIVITY AND SPATIAL FREQUENCY
In previous studies (7,8), bluegill sunfish proved to be excellent behavioral subjects, orienting promptly and accurately to visual stimuli that predict reward. Taking advantage of this behavior, we followed the recovery of contrast sensitivity to different spatial frequencies. Sunfish were trained to orient and swim to sinusoidal gratings patterns presented on one of two oscilloscopes at opposite ends of a rectangular tank. By requiring fish to orient first to a fixation light midway between the oscilloscopes, the viewing distance was set at 24 cm, and ensured that only one eye saw the onset of the grating pattern. Results from normal fish at a mean luminance of 25 cd/m2 yielded contrast sensitivity functions of conventional shape (6) peaking near 0.5 cycles per degree, and cutting off at 4.5 cycles per degree. Three sunfish kept at 25°C were trained preoperatively to gratings of low (0.15 cyclesfdeg), medium (1.0 cyclesfdeg) and high (2.93 cyclesldeg) spatial frequencies. The right optic nerve was then crushed intraorbitally and the fish tested on alternate days with all three spatial frequencies presented to each eye. We also administered blank trials containing neither stimulus nor reward in order to correct the data for response biases. In the three sunfish tested, responding via the crushed optic nerve was not seen until 64-70 days, when orienting abruptly reappeared to the low frequency grating at its maximum contrast of 0.5. The recovery of contrast sensitivity at the three spatial frequencies is shown in Fig. 3. Because each fish started responding at different times, their thresholds were averaged together by synchronizing the data from their respective times of first response (days of recovery). At the lowest spatial frequency, it took about 2 days for sensitivity to regain the normal range established by contemporaneous testing of the other eye, and 4-6 days at the middle spatial frequency. Contrast sensitivity at the high spatial frequency recovered much more gradually, without reliably reaching the normal range for at least 30 days into recovery. CONCLUSIONS
The goldfish psychophysics was consistent with the electrophysiology in that detection of positive disks returned at the same time that statistically significant
Mid Spatial Frequency (1 .O c/deg)
T 0
,i, I
, 10 Days of Recovery
loo
High Spatial Frequency (2.93 c/deg) *
2r--
Days of Recovery
0
FIG. 3. Psychophysical measurement of contrast sensitivity recovery in bluegill sunfish after crush of one optic nerve. The graphs show log contrast sensitivity to sinusoidal grating stimuli of spatial frequencies of 0.15, 1.00, and 2.93 cycles/degree at a mean luminance of 25 cd/m’. Each graph shows averaged contrast sensitivity obtained for three fish by synchronizing the data for each fish to the day that it first responded to gratings. Thus, the time axis is in terms of days of recovery on a logarithmic scale. Horizontal solid lines show mean contrast sensitivity via the control eye; dashed lines +2 standard deviations.
unit activity was first elicited in tectum by LED stimuli (40 days in goldfish) (4, 5). A similar correspondence was previously found for sunfish (7), in which behavioral orienting coincided with unit activity evoked in tectum by LED flashes (32-56 days postcrush). A second point of agreement was that positive disk detection always occurred later than negative disk detection in goldfish, although the psychophysics did not indicate as early a recovery for negative contrasts as the 20 days found electrophysiologically (4). This may mean that the visual channels conveying negative contrast in-
72
NORTHMORE
formation manifested in unit activity at 20 days are incapable of driving the behavioral responses studied here, at least until a more advanced stage of regeneration is reached around 30 days. In sunfish, recovery of grating detection was subject to the same long delay that occurred when this species was required to orient to LED flashes (7). If there is an earlier recovery of negative contrast channels, as found in goldfish, these channels seem unable to mediate responses to gratings. Figure 3 shows that after the abrupt onset of responding to gratings, contrast sensitivity was still somewhat depressed compared to control. There was then a gradual recovery to normal sensitivity which was noticeably slower at high spatial frequencies. The slowness of recovery may be related to the persistently low levels of visually evoked activity in the regenerating retinotectal system of sunfish (7). There is also a lingering fine-scale disorder in the regenerated retinotectal map that may impair sensitivity at high spatial frequencies (2, 11).
REFERENCES 1. HAYES, W. P., AND R. L. MEYER. 1988. Normal and regenerating optic fibers in goldfish tectum: HRP-EM evidence for rapid synaptogenesis and optic fiber-fiber affinity, J. Cqtp. Neural. 274: 516-538. 2. MEYER, R. L., K. SAKURAI, AND E. SCHAU~ECKER. 1985. Topography of regenerating optic fibers in goldfish traced with local wheat germ injections into retina: Evidence for discontinuous
AND CELENZA microtopography
in the retinotectal
projection. J. Comp. Neurol.
239:27-43. 3. NORTHMORE, D. P. M. 1984. Visual and saccadic activity in the goldfish torus longitudinalis. J. Comp. Physid. A. 155: 333-340. 4. NORTHMOFZE, D. P. M. 1989. Quantitative electrophysiological
5.
6. 7. 8. 9. 10. 11.
studies of regenerating visuotopic maps in goldfish. I. Early recovery of dimming sensitivity in tectum and torus longitudinalis. Neuroscience 32: 739-747. NORTHMORE, D. P. M. 1989. Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish. II. Delayed recovery of sensitivity to small light flashes. Neuroscience 32: 749-757. NORTHMORE, D. P. M., AND C. A. DVORAK. 1979. Contrast sensitivity and acuity of the goldfish. Vision Res. 19: 255-261. NORTHMORE, D. P. M., AND T. MASINO. 1984. Recovery of vision in fish after optic nerve crush: A behavioral and electrophysiological study. Enp. Neural. 84: 109-125. NORTHMORE, D. P. M., L. C. SKEEN, AND J. M. PINDZOLA. 1981. Visuomotor perimetry in fish: A new approach to the functional analysis of altered visual pathways. Vision Res. 21: 843-853. SPERRY, R. W. 1948. Patterning of central synapses in regeneration of the optic nerve in teleosts. Physid. Zool. 21: 351-361. SCHMIPT, J. T., AND D. L. EDWARDS. 1983. Activity sharpens the map during regeneration of the retinotectal projection in goldfish. Brain Res. 269: 29-39. SCHMIDT, J. T., J. C. TURCOTTE, M. BUZZARD, AND D. G. TIEMAN. 1988. Staining of regenerated optic arbors in goldfish tecturn: Progressive changes in immature arbors and a comparison of mature regenerated arbors with normal arbors. J. Comp. Neurol.
207:
565-591.
12. STUERMER, C. A. 0. 1988. Trajectories of regenerating retinal axons in the goldfish tectum. II. Exploratory branches and growth cones on axons at early regeneration stages. J. Comp. Neurol. 267: 69-91.
NEUROLOGY
115,69-72
(1992)
Recovery of Contrast Sensitivity during Optic Nerve Regeneration in Fish’ D.P.M. ~epurt~e~t
NORTHMOREAND
of ~sycko~gy and Neuroscience ~ogru~,
Psychophysical experiments on goldfish and sunfish studied the recovery time course of visual contrast detection during optic nerve regeneration. The results showed delayed recovery of detection of positive as compared to negative contrasts, and of high as compared to low spatial frequencies. The findings are related to previous electrophysiological and anatomical results in the fish retinotectal system. Q 1992 Academic Press,
Inc.
The teleost optic nerve readily regenerates after it is crushed. Behavioral tests, have tended to show virtually complete recovery of vision (7, 9), suggesting that regenerating optic nerve fibers eventually reestablish normal central connections. Anatomical studies in goldfish have shown that by about 20 days postcrush, the optic tectum contains regenerating optic axons with synapses upon tectal cells (1, 12). Many of these axons branch very extensively over the tectal surface. By about 40 days, optic terminal arbors are located at appropriate retinotopic positions over the tectal surface, with fewer arbors of large extent (2,ll). This process of refinement of the retinotectal map has also been studied electrophysiologically, mainly by recording visually evoked activity from optic nerve terminals in the superficial layers of tectum. Such recordings have found enlarged mult~unit receptive field (MURFs) that shrink to normal dimensions over time (10). Thus both anatomical and physiological approaches show that the retinotectal projections are refined by progressive shifting and reshaping of arbors. To assess the transmission of useful visual information by the regenerated retinotectal interface, we are currently using psychophysical methods to measure the contrast sensitivity of fish undergoing optic nerve regeneration. Our aims are to relate recovery to the changes in the retinotectal projection revealed anatomically and physiologically, and to see whether the various * This work Eye Institute
was supported of NIH.
by a grant
(EY02697)
from
the National
M.A.
CELENZA
Un~uers~ty of ~elu~~re,
visual information courses of recovery.
repark,
~eluware
channels
ELECTROPHYSIOLOGY:
19716
exhibit
MURF
different
time
REFINEMENT
Electrophysiological experiments in our laboratory have characterized MURFs quantitatively during optic nerve regeneration in goldfish (4, 5) using two kinds of stimuli differing primarily in the sign of their contrast. The first was an array of miniature, red light-emitting diodes (LEDs) that were flashed in the fish’s visual field; the second was a black vertical stripe (10’ wide) rotated slowly through the visual field. Both stimuli were presented against the same illuminated background at photopic levels (15 cd/m’). Figure 1 compares the widths of MURFs obtained with these two stimuli in different goldfish at various times after optic nerve crush. Using the black-stripe stimulus, visually evoked activity was first detected at about 20 days postcrush in tectum and in torus longitudinal& The latter is a nucleus with no direct retinal input that receives dimming information from tectal neurons (3). MURF widths were initially much enlarged but recovered gradually, approximated by an exponential decay with a time constant of 26 days. The LED stimuli, however, did not reliably evoke unit activity in tectum until about 40 days postcrush, although OFF responses could be observed with high-contrast stimulation. Several MURF characteristics, in addition to their widths (Fig. lB), showed that LED-sensitive MURFs, when they appeared, rapidly returned to normal. The results suggest that visual channels carrying dimming or OFF information recover first, followed by those carrying ON information. PSYCHOPHYSICS: POSITIVE AND CONTRAST SENSITIVITY
NEGATIVE
To see whether these differences in recovery time observed electrophysiolo~cally represent ~~~ctio~l reconnection of different information channels, goldfish were tested psychophysically for their ability to detect both positive and negative contrast stimuli during optic nerve regeneration. Goldfish were kept at 25°C and classically condi69
0014-4886/92
$3.00
Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.
70
NORTHMORE NEGATIVE
CONTRAST
STIMULI
500 400
-
0
TECTUM
.
TL
,-_------------------~_~_ 0 ’ 0
__,
I
I
I
I
I
I
20
40
60
80
100
120
POSITIVE
CONTRAST
I 140
STIMULI
AND
CELENZA
dures were programmed for each stimulus type, such that after a hit trial, disk contrast was lowered by 0.25 log unit for the next presentation of that stimulus, otherwise it was raised by 0.25 log unit. Fish were typically tested every other day. Figure 2 compares the detection recovery of negative and positive contrast disk stimuli (1.6” diam) presented to the crushed side of one goldfish. The upper half of each figure shows suppression ratios in each trial. Values around 1.0 indicate no response to the negative disk stimuli until about 30 days for negative contrast, and 39 days for positive disks. The lower halves of each figure show how disk contrast tracked the fish’s contrast
(Ofl(mj
200 ------
~~~I~--~-~~~-------~-~~-
100 0'
L----------------------I 0 20
I 40
4 60 DAYS
I 80 POSTCRUSH
1 100
I 120
0
1 I 140
FIG. 1. Electrophysiological determinations of recovery of multiunit receptive field (MURF) dimensions in the goldfish visual system after crushing one optic nerve. The half-maximum widths of MURFs recorded from tectum or torus longitudinalis (TL) are shown as a percentage of control values. Horizontal dashed lines show f2 standard deviations. Upper: Activity was evoked by a 10’ wide vertical black stripe moving slowly through the visual field. Each data point is the mean of several MURFs recorded from one fish. Lower: Stimuli were flashed red LEDs. Data are from individual receptive fields yielding multiunit activity that was statistically discriminable from background activity.
tioned to visual stimuli using respiration suppression as the conditioned response (6). Fish were restrained in a holder such that one eye faced a video display screen (23 x 20 ems) at an apparent underwater distance of 44 ems. A motor rotated the fish holder to allow testing of either eye. A thermistor in front of the mouth was used to monitor respiration amplitude and frequency. Between trials, the display screen showed a neutrally colored, uniform background of 30 cd/m2; during a trial, one of four types of stimulus disk, 1.6 or 16” diam of either positive or negative contrast, was presented in the screen center for 5 s. Suppression of respiration was conditioned by pairing the offset of the stimulus disk (log contrast = -0.25) with mild electric shock to the tail. After training fish to a criterion using left and right eyes in alternation, one optic nerve was crushed intraorbitally. A computer presented the different stimuli in random order, rotated the fish to test the crushed or uncrushed side, and scored a hit if respiration amplitude was suppressed by more than 50%. In order to track contrast thresholds over time, separate staircase proce-
0
10
20
30
40
50
50
70
80
90
1 K)
6 1.53
I
0
10
20
30
40
50
60
70
80
so
loo
DAYS POSTCRUSH FIG. 2. Psychophysical determination of the time course of recovery of contrast detection in one goldfish using its regenerating optic nerve. Stimuli were 1.6” disks, either negative contrast (A) or positive contrast (B). The upper halves of each figure show respiration suppression ratios calculated as the mean respiration amplitude during the stimulus presentation, divided by the mean amplitude over 15 s before stimulus presentation. A value of 1.0 indicates no suppression response; 0.0, full suppression response. Lower halves show trial-by-trial stimulus contrast tracked by a staircase procedure. The continuous horizontal lines show the mean contrast threshold of the control eye obtained at the same time.
VISUAL
CONTRAST
RECOVERY
IN
71
FISH
Low Spatial Frequency (0.15 c/deg)
threshold. For both negative and positive disks, threshold followed a downward trend, reaching control levels only after about 70 days postcrush. Similar trends were also found for the large (16”) disks. In five other goldfish tested so far, negative contrasts were detected about 10 days before positive contrasts.
---
2l--
PSYCHOPHYSICS: CONTRAST SENSITIVITY AND SPATIAL FREQUENCY
In previous studies (7,8), bluegill sunfish proved to be excellent behavioral subjects, orienting promptly and accurately to visual stimuli that predict reward. Taking advantage of this behavior, we followed the recovery of contrast sensitivity to different spatial frequencies. Sunfish were trained to orient and swim to sinusoidal gratings patterns presented on one of two oscilloscopes at opposite ends of a rectangular tank. By requiring fish to orient first to a fixation light midway between the oscilloscopes, the viewing distance was set at 24 cm, and ensured that only one eye saw the onset of the grating pattern. Results from normal fish at a mean luminance of 25 cd/m2 yielded contrast sensitivity functions of conventional shape (6) peaking near 0.5 cycles per degree, and cutting off at 4.5 cycles per degree. Three sunfish kept at 25°C were trained preoperatively to gratings of low (0.15 cyclesfdeg), medium (1.0 cyclesfdeg) and high (2.93 cyclesldeg) spatial frequencies. The right optic nerve was then crushed intraorbitally and the fish tested on alternate days with all three spatial frequencies presented to each eye. We also administered blank trials containing neither stimulus nor reward in order to correct the data for response biases. In the three sunfish tested, responding via the crushed optic nerve was not seen until 64-70 days, when orienting abruptly reappeared to the low frequency grating at its maximum contrast of 0.5. The recovery of contrast sensitivity at the three spatial frequencies is shown in Fig. 3. Because each fish started responding at different times, their thresholds were averaged together by synchronizing the data from their respective times of first response (days of recovery). At the lowest spatial frequency, it took about 2 days for sensitivity to regain the normal range established by contemporaneous testing of the other eye, and 4-6 days at the middle spatial frequency. Contrast sensitivity at the high spatial frequency recovered much more gradually, without reliably reaching the normal range for at least 30 days into recovery. CONCLUSIONS
The goldfish psychophysics was consistent with the electrophysiology in that detection of positive disks returned at the same time that statistically significant
Mid Spatial Frequency (1 .O c/deg)
T 0
,i, I
, 10 Days of Recovery
loo
High Spatial Frequency (2.93 c/deg) *
2r--
Days of Recovery
0
FIG. 3. Psychophysical measurement of contrast sensitivity recovery in bluegill sunfish after crush of one optic nerve. The graphs show log contrast sensitivity to sinusoidal grating stimuli of spatial frequencies of 0.15, 1.00, and 2.93 cycles/degree at a mean luminance of 25 cd/m’. Each graph shows averaged contrast sensitivity obtained for three fish by synchronizing the data for each fish to the day that it first responded to gratings. Thus, the time axis is in terms of days of recovery on a logarithmic scale. Horizontal solid lines show mean contrast sensitivity via the control eye; dashed lines +2 standard deviations.
unit activity was first elicited in tectum by LED stimuli (40 days in goldfish) (4, 5). A similar correspondence was previously found for sunfish (7), in which behavioral orienting coincided with unit activity evoked in tectum by LED flashes (32-56 days postcrush). A second point of agreement was that positive disk detection always occurred later than negative disk detection in goldfish, although the psychophysics did not indicate as early a recovery for negative contrasts as the 20 days found electrophysiologically (4). This may mean that the visual channels conveying negative contrast in-
72
NORTHMORE
formation manifested in unit activity at 20 days are incapable of driving the behavioral responses studied here, at least until a more advanced stage of regeneration is reached around 30 days. In sunfish, recovery of grating detection was subject to the same long delay that occurred when this species was required to orient to LED flashes (7). If there is an earlier recovery of negative contrast channels, as found in goldfish, these channels seem unable to mediate responses to gratings. Figure 3 shows that after the abrupt onset of responding to gratings, contrast sensitivity was still somewhat depressed compared to control. There was then a gradual recovery to normal sensitivity which was noticeably slower at high spatial frequencies. The slowness of recovery may be related to the persistently low levels of visually evoked activity in the regenerating retinotectal system of sunfish (7). There is also a lingering fine-scale disorder in the regenerated retinotectal map that may impair sensitivity at high spatial frequencies (2, 11).
REFERENCES 1. HAYES, W. P., AND R. L. MEYER. 1988. Normal and regenerating optic fibers in goldfish tectum: HRP-EM evidence for rapid synaptogenesis and optic fiber-fiber affinity, J. Cqtp. Neural. 274: 516-538. 2. MEYER, R. L., K. SAKURAI, AND E. SCHAU~ECKER. 1985. Topography of regenerating optic fibers in goldfish traced with local wheat germ injections into retina: Evidence for discontinuous
AND CELENZA microtopography
in the retinotectal
projection. J. Comp. Neurol.
239:27-43. 3. NORTHMORE, D. P. M. 1984. Visual and saccadic activity in the goldfish torus longitudinalis. J. Comp. Physid. A. 155: 333-340. 4. NORTHMOFZE, D. P. M. 1989. Quantitative electrophysiological
5.
6. 7. 8. 9. 10. 11.
studies of regenerating visuotopic maps in goldfish. I. Early recovery of dimming sensitivity in tectum and torus longitudinalis. Neuroscience 32: 739-747. NORTHMORE, D. P. M. 1989. Quantitative electrophysiological studies of regenerating visuotopic maps in goldfish. II. Delayed recovery of sensitivity to small light flashes. Neuroscience 32: 749-757. NORTHMORE, D. P. M., AND C. A. DVORAK. 1979. Contrast sensitivity and acuity of the goldfish. Vision Res. 19: 255-261. NORTHMORE, D. P. M., AND T. MASINO. 1984. Recovery of vision in fish after optic nerve crush: A behavioral and electrophysiological study. Enp. Neural. 84: 109-125. NORTHMORE, D. P. M., L. C. SKEEN, AND J. M. PINDZOLA. 1981. Visuomotor perimetry in fish: A new approach to the functional analysis of altered visual pathways. Vision Res. 21: 843-853. SPERRY, R. W. 1948. Patterning of central synapses in regeneration of the optic nerve in teleosts. Physid. Zool. 21: 351-361. SCHMIPT, J. T., AND D. L. EDWARDS. 1983. Activity sharpens the map during regeneration of the retinotectal projection in goldfish. Brain Res. 269: 29-39. SCHMIDT, J. T., J. C. TURCOTTE, M. BUZZARD, AND D. G. TIEMAN. 1988. Staining of regenerated optic arbors in goldfish tecturn: Progressive changes in immature arbors and a comparison of mature regenerated arbors with normal arbors. J. Comp. Neurol.
207:
565-591.
12. STUERMER, C. A. 0. 1988. Trajectories of regenerating retinal axons in the goldfish tectum. II. Exploratory branches and growth cones on axons at early regeneration stages. J. Comp. Neurol. 267: 69-91.
