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Learning and interocular transfer of visual discriminations by goldfish with retinotectal compression
EXPERIMENTAL
NEUROLOGY
I3 (1985)
88,696-7
Learning and Interocular Transfer of Visual Discriminations by Goldfish with Retinotectal Compression A.A.DuNN-MEYNELLANDG. Department
of Biology,
Queen
Mar?,
College,
Received
August
I. 1984; revision
E. SAVAGE'
Mile
End Road,
received
January
London,
England
El
4NS
28. 1985
Visual function mediated by a compressed retinotectal projection was examined by training goldfish with unilateral retinotectal compression to perform red/green and horizontal/vertical discriminations. Fish were trained monocularly via the compressed or the normal visual field using an aversive classical conditioning model. Interocular transfer was then examined to determine if the mechanisms mediating this transfer functioned normally after retinotectal compression and to compare interpretation of visual information via normal and compressed visual fields. Both visual discriminations were learned successfully using the normal or the compressed visual field. Learning deficits (relative to controls) were, however, observed in fish trained with the color discrimination using the compressed visual field. or the horizontal/vertical discrimination using the compressed or the normal visual field. Interocular transfer of the color discrimination from the compressed to the normal visual held or in the reverse direction was demonstrated to occur at approximately normal values. Interocular transfer of the horizontal/vertical discrimination was successful from the compressed to the normal visual field. but was reduced or absent in the opposite direction. The results indicate that analysis of the colors red and green is essentially normal after retinotectal compression, and that the pathways mediating interocular transfer of this color discrimination remain functional. There were, however, abnormalities in the mechanism mediating interocular transfer of pattern discriminations after retinotectal compression. 0 1985 Academic Press. Inc.
INTRODUCTION In teleost fish the vast majority in the optic tectum contralateral
of retinal ganglion cell fibers terminate to the eye of origin. This retinotectal
Abbreviations: DL-discrimination level, PD-percentage deceleration. i All correspondence should be sent to A.D.M. at his present address: Ophthalmology, New York Medical College, Valhalla, NY 10595.
696 0014-4886/85
$3.00
Copynghl 0 1985 by Academic Press, Inc. All tights of reproduction in any form reserved.
Department
of
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projection is topographically ordered so that ganglion cells serving different areas of the visual field terminate at different positions in the tectum. The retinotectal projection is capable of showing a variety of forms of plasticity after surgical manipulation in adult fish. For example, if the caudal half of one tectum is removed, most or all of the ganglion cells previously projecting across the whole tectum come to project across the remaining half-tectum, a process known as retinotectal compression [see, for example, (4, 5, 12)]. Most studies of plasticity in the teleost visual system utilized electrophysiologic or anatomic techniques to examine the pattern of projection of ganglion cell fibers on the tectum. Little information is available with regard to changes in other portions of the central nervous system (including the tectal cells themselves) in response to changes in the retinotectal projection that follow tectal surgery. Our knowledge of whether or not altered retinal connections are capable of mediating normal perception and appropriate responses to visual stimuli is therefore relatively sparse. A few studies, however, have been conducted on the behavior of fish with compression of the visual field. Those studies demonstrated that the altered visual system is functional for guidance of motor activity (13) and for discrimination on the basis of orientation (8, 22, 26), color (17, 18), or intensity (26). In this paper we describe experiments that examined the ability of fish with unilateral retinotectal compression to perform interocular transfer of visual discriminations. Interocular transfer is the process by which learned responses to visual discriminations acquired using one eye may be demonstrated when stimuli are presented to the opposite eye. In goldfish, very few, if any retinal fibers project to the ipsilateral optic tectum (19, 2 1). Therefore, if a visual discrimination is presented in the monocular portion of one visual field, detailed visual information is relayed to only one half of the brain. For interocular transfer to occur, the visual information must be passed to the other brain half via the commissures linking the two sides of the brain. Francis et al. (3) showed that interocular transfer remained possible after regeneration of a crushed optic nerve. However, in experiments described in an unpublished manuscript, Campbell, Hope, and Ingle failed to demonstrate interocular transfer of pattern discriminations in fish with retinotectal compression. If this latter result proves correct, it would indicate a previously unsuspected abnormality in tectal connections after partial tectal ablation and visual field reorganization. Alternatively, if this observation were incorrect, interocular transfer in fish with unilateral retinotectal compression will provide an excellent system for comparison of the analysis of visual information between normal and compressed visual fields. In addition to examining the feasibility of interocular transfer, our experiments allow a reexamination of the effects of retinotectal compression on learning. Previous studies have been contradictory over whether or not
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partial tectal ablation and visual acquisition of visual discriminations
AND
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field compression (22, 26).
leads to deficits
in
METHODS The experiments were carried out on 7- to 1 l-cm goldfish (Curassius LZWU~US) which were kept under a 15-h light:9-h dark schedule at 17 to 21°C. Partial tectal ablations were carried out on each of 46 fish using the following methodology: The fish was anesthetized with MS222 solution which was then passed over the gills to maintain anesthesia. A flap of cranium was removed to reveal one tectal lobe. Using a sharpened tungsten needle, an incision about 300 /*rn deep was made in the tectum. The incision extended from the dorsomedial to the ventrolateral edge of the tectal lobe, splitting the tectum into rostra1 and caudal halves. The caudal half was then removed by aspiration. After this the cranial flap was glued back into place and the fish was revived. In each of a further 11 fish, sham operations were made. These fish were anesthetized and the cranium was opened as described, and then the cranium was resealed without tectal surgery and the animals were revived. All fish (including the sham-operated controls) were then left 3.5 to 22 months before further use. Maps of the retinotectal projection were made of 21 of the fish with partial tectal ablations (six of these fish were also trained with one of the visual discriminations) and of 15 unoperated controls. To map the projection, the fish was anesthetized, its cranium was opened, and the animal was positioned at the center of a visual perimeter. For each of a series of points on the optic tectum (Figs. 1 and 2), an extracellular electrode was lowered into the tectal lobe. Multicellular potentials were recorded with the electrode as a slowly flashing light was moved over the visual perimeter. The point at which the light elicited most activity was then noted, before the electrode was moved to the next tectal locus. The fish were trained using classical conditioning of their cardiac deceleratory response to aversive stimuli. The electrocardiogram (ECG) was recorded by electrodes implanted using the methods of Roberts et at. (15). Briefly, the fish was anesthetized and the scales were scraped from a small patch of skin on its ventral aspect between the pectoral fins. Electrodes were then implanted through the bared patch so that their tips lay adjacent to the pericardium, and were glued in place, before the fish was revived; 1 h for postoperative recovery elapsed before the start of training. After implantation of the electrodes, the fish was restrained in a plasticmesh envelope. Thus immobilized, the animal was placed in a T-shape black Perspex Chamber. The base of the T (in which the fish was held)
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measured 14 cm long X 3 cm wide X 6 cm deep. The front 4 cm of this chamber was open to the side arms which were 8 cm long X 4 cm wide X 6 cm deep. The animal was positioned so that the left eye had an unrestricted view into the left arm of the T and the right eye into the right arm. Neither eye could see into the arm on the opposite side. The visual stimuli were presented at the end of the side arms during training. An opaque cover was placed over the training chamber to prevent the fish from viewing the stimuli except when they were in place, or from seeing the experimenter. The chamber was suspended in a tank containing water at 19 to 2 1“C. The subject’s ECG was recorded with a Washington MD2 pen recorder and passed to a microprocessor that counted heart beats. The microprocessor also controlled trial onset and delivered shock reinforcement through a pair of copper plates adjacent to the fish’s tail. Each subject was trained to perform either a color (red/green) or an orientation (horizontal/vertical) discrimination. The stimuli used for training the color discrimination were 2-cm-diameter disks of plastic painted with Humbrol Emerald Green gloss paint, or Humbrol Brilliant Red gloss paint. The orientation discrimination was trained using 1.5- X 0.5-cm bars of white plastic mounted horizontally or vertically. All stimuli were mounted on the end of matt black wires. Three groups of fish were trained with each of the two discriminations: operated controls (cant); fish with retinotectal compression trained using the normal visual projection (RTC-norm) and fish with retinotectal compression trained with the compressed projection (RTC-camp). The color discrimination was trained to 5 controls, 5 fish with retinotectal compression trained with the normal visual field, and 6 fish trained with the compressed visual field. The orientation discrimination was trained to 6 controls, 7 fish with tectal surgery trained with the normal visual field, and 13 fish trained with the compressed field. Half an hour before commencing training, the subject was placed in the apparatus. Before training began, the AC electric shock was adjusted to an intensity sufficient to produce an unconditioned response of a cardiac deceleration of approximately 50% for 4 s after shock application. Each subject was trained monocularly using the same eye throughout habituation and training trials. In an individual trial, the number of heart beats was counted for 10 s, and then one of the stimuli was presented at the end of one side arm for 10 s, while the heart beats were again counted. During presentation, the stimulus was bobbed up and down through approximately 2 cm at one up-down cycle per second. At the end of the presentation period, before the stimulus was removed from the side arm, a 0.5-s electric shock was delivered if appropriate. Trials were given every 120 + 30 s. Each fish was trained in a single session of 130 trials. Training began
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with 20 habituation trials during which no electric shocks were given. During these habituation trials, as well as throughout the training trials, the stimulus order followed a semirandom, Gellerman sequence (6). After the habituation trials, the stimulus that had elicited least unconditioned cardiac deceleration was designated reinforced (+) and was followed by shock during the training trials. The other stimulus was designated unreinforced (-) and was not followed by shock. One hundred training trials were then given, followed by 10 unreinforced transfer trials with the stimuli presented to the naive eye. During the transfer trials the stimuli were presented in the sequence -++--++--+. During training, the conditioning results were analysed by the microprocessor as follows: For each trial, the number of heart beats during the 10 s before stimulus presentation (PRE) and the number of heart beats occurring during the 10-s presentation period (DUR) were counted. The percentage deceleration of the heart rate in response to the stimulus (PD) was then calculated as: PD = ((PRE - DUR)/PRE) X 100%. A positive value for this measure indicated a deceleration of the heart and a negative value indicated the opposite. To quantify the subject’s performance of the discrimination between the two stimuli, the discrimination level (DL) was calculated. The data were divided into 10 trial blocks. For each block, the average percentage decelerations in response to the stimulus that was reinforced during the training trials (PD+) and in response to the negative stimulus (PD-) were calculated. The DL was then derived for each IO-trial block using the following equation: DL = ((PD+ - PD-)/(PD+ + PD-)) X 100%. A positive DL indicated that the subject responded more to the reinforced stimulus than to the unreinforced one, and a negative DL indicated the reverse. Because the above equation yielded meaningful results only when PD- and PD+ were positive, an arbitrary DL was assigned when negative PDs occurred (that is, when the heart rate increased in response to the stimulus, a very rare event). If both PD- and PD+ were negative, then a DL of zero was assigned for that lo-trial block. If only PD’ was negative, the greatest negative DL observed in that animal prior to the IO-trial block concerned was assigned (or zero if no negative DL had been observed). Similarly, the greatest positive DL or zero was assigned if only PD- was negative. To quantify the rate of acquisition of the discrimination, a trials-tocriterion measure was calculated. The criterion level for each of the two tasks was set as one-half the overall average DL for the last 50 training trials in the control group trained with the corresponding task. This gave a DL of 2 1.1% for the color discrimination and 13.1% for the orientation discrimination. Moving averages were then calculated for the training data of each animal, averaging three IO-trial blocks. The first trio of IO-trial
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blocks in which the average DL exceeded the criterion DL was taken as the point at which criterion was attained, and the trials to criterion was set for that animal as the last trial in those three blocks. Thus if the DLs that a subject gave in the first, second, and third lo-trial blocks after training began were greater than the criterion level when averaged together, 30 trials to criterion was recorded. If not, the DLs of the second, third, and fourth lo-trial blocks were averaged and 40 trials to criterion was recorded if the criterion was attained. If criterion was not attained during the 100 training trials, 110 trials to criterion was arbitrarily assigned. RESULTS Evidence of visual field compression was seen in all retinotectal maps of fish with partial tectal ablations. Examples of normal and compressed retinotectal maps are shown in Fig. 1 and 2, respectively. The results from animals trained with the color discrimination are described first. Table 1 shows the average percentage decelerations in response to the reinforced and unreinforced stimuli. These figures are for each of the three treatment groups and for each lo-trial block. Because evidence of learning was biased against by the selection of the stimulus eliciting least unconditioned response during habituation as the reinforced stimulus, DL values significantly above zero demonstrated that learning had occurred. To yield a single measure of the degree of discrimination displayed by each animal by the end of training, the DLs from the last three lo-trial blocks before testing for interocular transfer were averaged for each subject. This average was termed the DLtrain. The DLtrains of each group of fish were statistically tested to determine if they were significantly above zero. One-tailed Wilcoxon matched-pair signed ranks tests were used for this purpose (for this test the DLtrain was treated as the difference between a matched pair of observations, the relative response to reinforced and unreinforced stimuli). These tests showed that all groups had DLtrains significantly above zero and had therefore learnt the discrimination (Cont: N = 5; T = 0; P < 0.05. RTC-norm: N = 5; T = 0; P < 0.05. RTC-camp: N = 6; T = 0; P < 0.025). The average DLtrains f SE for the animals trained with the color discrimination are shown in Fig. 3. The DLtrains of the control fish were compared with the fish in the other two groups using one-tailed Wilcoxon rank sum tests. These tests showed that neither of the experimental groups had DLtrains significantly lower than the controls (RTC-norm: M = 5; N = 5; T = 24.5; P > 0.05. RTC-camp: A4 = 5; N = 6; T = 35; P > 0.05). The trials-to-criterion results for fish trained with the color discrimination are shown in Fig. 4. The fish with unilateral retinotectal compression
702
DUNN-MEYNELL LEFT
VISUAL
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FIELD SUPERIOR
IWFElllOll
RIGHT
TECTUM LATERAL
FIG. I. The retinotectal map of a control fish. At the top of the figure is shown a representation of the subject’s left visual field. Below is a diagram of the dorsal surface of the right tectal lobe. Nervous activity was recorded from an electrode lowered into each of the loci indicated on the tectal diagram by numbers. The numbers in the visual field diagram indicate the positions at which a visual stimulus elicited maximum response recorded at the correspondingly numbered electrode positions. Electrode positions running rostrocaudally along the tectum and their corresponding visual field positions are joined by lines to ease interpretation of the diagram. The edge of the visual field diagram extends I IO” from its center.
trained by the normal visual field learned slightly more slowly than the controls; however, the difference in trials to criterion was not significant (A4 = 5, N = 5, T = 30, P > 0.05). The fish trained by the compressed visual field, however, required a significantly greater number of trials to criterion than did the controls (A4 = 5, N = 6, T = 19, P < 0.025). These significances were calculated using one-tailed Wilcoxon rank sum tests. In both groups with retinotectal compression, the average DL during the interocular transfer trials (DLtransfer) was significantly above zero (calculated
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LEFT
INCENIOR
RIGHT
TECTUM
LATERAL
FIG. 2. The retinotectal map of a fish with a compressed visual field. The shaded portion of tectum had been ablated.
using one-tailed Wilcoxon matched-pairs signed rank tests; RTC-norm: M = 5; T = 0; P < 0.05. RTC-camp: A4 = 6; T = 2; P < 0.05). This demonstrated the success of interocular transfer in the two experimental groups. Due to equipment malfunction, the interocular transfer data were lost from one control animal. Consequently a Wilcoxon matched-pairs signed ranks test could not be used here (because this test cannot prove significance at the 0.05 level with less than five values). However, the DLtransfer of the controls was well above zero (Fig. 3) and the standard error was relatively small, strongly implying that transfer was also successful in this group. In evaluating the degree of interocular transfer it is of little value to compare directly the DLtransfer levels of groups that attained different levels of discrimination at the end of training. A more meaningful measure is the ratio of discrimination level during the transfer trials relative to the
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AND TABLE
Average
Percentage
1 2 3 4 5 6 7 8 9 10 11 12 13
1
Decelerations in Response to Reinforced and Unreinforced by Fish Trained with the Color Discrimination” Cont
1O-Trial block
SAVAGE
RTC-norm
RTC-camp
Unreinforced
Reinforced
Unreinforced
Reinforced
Unreinforced
23.5 20.7 8.9 6.1 18.2 29.6 29.6 25.2 20.1 18.4 14.4 9.8 15.7
21.4 10.0 6.5 21.6 30.0 43.3 43.6 47.5 39.4 33.7 38.2 34.0 37.4
35.9 10.2 8.9? 30.6 26.7 27.2 29.3 32.8 24.7 24.2 20.9 21.0 27.6
26.0 10.2 23.7* 43.2 46.0 52.3 54.9 57.8 62.2 63.3 62.7 57.9 48.4
40.2 26.5 21.2? 13.9 24.0 38.3 31.0 41.8 37.5 28.4 37.0 32.3 32.5
f 8.4 + 8.9 f 8.2 f 5.6 + 6.8 k 11.7 + 10.8 + 8.3 + 11.3 + 8.1 ? 7.0 k 4.0 k 4.3
f f 2 f + + f f + f + f -c
4.1 10.2 2.6 5.8 12.3 16.6 14.3 11.1 12.1 9.6 12.9 9.3 9.7
f f f f f k + + + + + +
4.3 4.1 5.2 8.7 9.0 9.7 10.0 9.8 8.4 7.9 9.7 9.7 9.2
Stimuli
f f + k + + f + f + f +
3.2 4.9 5.1 10.0 10.6 11.4 11.9 6.8 7.1 6.0 8.7 10.7 8.6
f 7.4 +- 8.6 7.6 f 4.9 + 7.1 f 11.2 f 11.2 f 10.6 f 8.6 f 5.9 f 7.5 f 8.4 f 4.6
Reinforced 40.5 10.5 19.1 14.7 32.7 45.0 42.5 50.4 57.3 59.1 54.3 59.1 47.4
f f f f f f f + f + -t f k
7.2 6.4 10.1 13.5 9.6 14.0 14.3 12.2 10.4 7.2 7.7 6.2 7.0
’ For each animal, the responses to the stimulus that was reinforced during training and to the negative stimulus were averaged within each lo-trial block. These values were then used to calculate the mean responses to the two stimuli f SE for each experimental group in each lotrial block. The first two lo-trial blocks were the habituation trials. the next 10 blocks were the training trials, and the last block was the transfer trials. Cont-controls. RTC-norm-fish with unilateral retinotectal compression trained on the normal visual field and tested for interocular transfer using the compressed visual field. RTC-camp-fish trained on the compressed visual field and tested for interocular transfer using the normal visual field.
level at the end of training, i.e., (DLtransfer/DLtrain) X 100%. Such a measure was used by Yeo and Savage (24) and termed the “transfer level.” A transfer level of 100% indicates that the discrimination was performed equally well before and after transfer. A transfer level of 0% would indicate a complete failure of interocular transfer (equal response to both stimuli on transfer testing). The three groups trained with the color discrimination attained the following transfer level (X + SE): cant, 81.5 + 28.9%; RTC-norm, 62.2 + 8.7%; RTC-camp, 69.7 + 47.3%. Thus the two groups with retinotectal compression showed transfer level similar to, though slightly lower than that observed in controls. The difference in transfer levels between the controls and the fish with retinotectal compression were not statistically significant (calculated using two-tailed Wilcoxon rank sum tests: RTC-
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r*n* Cont
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705
7
tr.,n RTC-norm
RTC-camp
FIG. 3. The group average discrimination levels + SE during the last 30 training trials (train) and during the transfer trials (trans) for the three groups trained with the color discrimination. Con&controls. RTC-norm-animals with unilateral retinotectal compression trained on the normal visual field and tested for interocular transfer on the compressed visual field. RTCcamp-fish with retinotectal compression trained on the compressed visual field and tested for interocular transfer on the normal visual field.
norm: M = 4; N = 5; T = 2 1; P > 0.05. RTC-camp:
M = 4; N = 6; T
= 27; P > 0.05). A similar set of analyses was carried out on the data obtained from fish trained with the horizontal/vertical discrimination. The average percentage decelerations in response to the two stimuli are shown in Table 2. Subjects in all three groups successfully acquired the orientation discrimination. This was demonstrated by the DLtrains of the subjects in each group (shown in Fig. 5) which were significantly above zero (cant: N = 6; T = 0; P < 0.025. RTC-norm: N = 7; T = 0; P c 0.0025. RTC-comp: N = 13; T = 5; P < 0.005). The group of fish with retinotectal compression trained on the compressed visual field attained a significantly lower DLtrain than the controls (M = 6, N = 13, T = 79, P = 0.05). The animals with retinotectal compression trained on the normal visual field did not differ significantly in DLtrain from the controls (M = 6, N = 7, T = 42, P > 0.05). The trialsto-criterion measure, however, showed that both groups with retinotectal compression learned significantly more slowly than the controls (RTC-
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loo9080. ; E
70.
= ; 0 0 c
00.
M
40.
: (E c
30.
50.
2010-
RTCnorm
RTCcamp
FIG. 4. The group average trials to criterion 2 SE for the three groups trained with the color discrimination. Cont-controls. RTC-norm-animals with retinotectal compression trained on the normal visual field. RTC-comp-fish with retinotectal compression trained on the compressed visual field.
norm: A4 = 6; N = 7; T = 27.5; P < 0.025. RTC-camp: M = 6; N = 13: T = 3 1; P = 0.005). The group average trials-to-criterion and SE are shown in Fig. 6. Both the controls and the animals with retinotectal compression trained on the compressed visual field were demonstrated to show interocular transfer of the visual discrimination as their DLtransfers were significantly above zero (cant: N = 6; T = 0; P < 0.025. RTC-camp: N = 13; T = 15.5; P < 0.025). However, the average DLtransfers of the fish with retinotectal compression trained on the normal visual field were not significantly above zero (N = 7, T = 14, P > 0.05). The average transfer levels confirmed that transfer was successful in controls (transfer level 72.2 k 24.9%) and in fish with retinotectal compression trained on the operated tectum (113.4 + 73.5%). The transfer levels of the fish in these two groups did not differ significantly (M = 6, N = 13, T = 58, P > 0.1). The transfer level of the fish with retinotectal compression trained on the normal visual field and tested for interocular transfer on the compressed visual field was, however, slightly below zero (-5.9 + 20.1%) suggesting a complete failure of interocular transfer. The difference in transfer levels between fish in this group and the controls was statistically significant (M = 6, N = 7, T = 56, P < 0.05).
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TABLE 2 Average Percentage Decelerations in Response to Reinforced and Unreinforced Stimuli by Fish Trained with the Horizontal/Vertical Color Discrimination” Cont 1O-Trial block 1 2 3 4 5 6 7 8 9 10 11 12 13
Unreinforced 16.4 + 8.1 + -6.6 k 19.3 f 27.4 f 25.7 + 23.8 f 31.0 f 40.3 f 37.5 f 40.7* 32.4 f 29.4 +
7.8 3.8 7.1 3.1 4.3 3.1 5.0 6.2 7.8 8.4 6.5 5.1 6.0
RTC-norm
RTC-camp
Reinforced
Unreinforced
Reinforced
16.5 f 5.6 6.0 + 3.7 3.6 f 7.3 24.7k4.0 33.8 + 3.8 34.6 f 3.9 33.6 + 4.2 48.3 + 8.0 55.4 + 7.2 60.0 f 8.0 58.6 + 5.7 63.1 + 6.0 41.3 + 9.4
27.1 + 6.9 13.9 I~I 5.6 5.3 f 5.2 11.3? 4.1 21.3 f 7.1 41.6 + 10.0 41.5 + 9.8 39.4 + 9.4 38.1 + 8.2 29.2 + 8.2 37.8 + 6.9 29.3 f 7.1 35.7 f 7.8
20.0 4.3 8.2 7.7 13.9 43.5 38.9 47.9 44.1 45.3 55.9 52.5 37.3
+ + f + + f f + f + f f +
6.0 8.1 2.9 5.0 8.0 11.9 8.4 8.4 8.8 9.7 8.6 7.7 7.1
Unreinforced 26.1 25.6 16.2 24.1 30.5 33.1 34.8 33.3 38.8 38.5 35.8 39.3 36.1
+ + f + + + + + + + + + +
5.2 5.1 5.2 4.7 4.9 5.1 4.7 4.3 5.0 4.6 5.6 4.8 4.4
Reinforced 19.8 21.0 15.7 25.6 32.1 36.6 38.5 43.9 41.7 48.3 46.4 54.3 46.0
f f f f f f f f f f + f f
5.5 5.1 5.0 3.7 5.0 6.5 5.7 5.8 6.7 6.0 6.9 6.7 4.9
a Calculations were performed as described for Table 1. Cont-controls. RTC-norm-fish with unilateral retinotectal compression trained using the normal visual field and tested for interocular transfer via the compressed visual projection. RTC-comp-fish with retinotectal compression trained by the compressed field and tested via the normal field.
DISCUSSION Our results confirm that color and horizontal/vertical discriminations may be learned by goldfish with unilateral retinotectal compression on the normal or the compressed visual field. We demonstrate, however, that deficits occur in the acquisition of either discrimination on the compressed visual field and of the orientation discrimination on the normal visual field. We also show that interocular transfer of the color discrimination is possible both to and from the brain half with retinotec@ compression. However, interocular transfer of the orientation discrimination could be proven only from the compressed to the normal visual projection. Our demonstration that a red/green discrimination may be learned on a compressed visual field confirms Scott’s finding (17, 18). Previous studies have shown that normal goldfish learn a red/green discrimination on a color rather than an intensity basis. This was originally demonstrated by McCleary and Bernstein (11) and was confirmed by Sienkiewicz (20). Sienkiewicz presented the stimuli in the same manner as we employed and his training stimuli were colored identically to those that we used. In
35
30
5 Y -I z 0 ; e z
15
I10 Le 0 m -0
;
f
20
Ii
5
?
0 25 I -5
Cont
J
train
trans
RTC-norm trans train
!!!
RTC-camp tran* train
FIG. 5. The average discrimination levels + SE for the last 30 training trials (train) and for the transfer trials (trans) in the groups trained to perform the orientation discrimination. Cont-controls. RTC-norm-fish with retinotectal compression trained using the normal visual field and tested for interocular transfer on the compressed visual field. RTC-camp-fish with retinotectal compression trained using the compressed visual field and tested for interocular transfer on the normal visual field.
90
so
iE ;
70
F ; 0
aa
0 c a : ; c
I
50 40 30 20
norm CObVlP FIG. 6. Group average trials to criterion + SE for the groups trained with an orientation discrimination. Cont-controls. RTC-norm-animals with retinotectal compression trained using the normal visual field. RTC-camp-fish with retinotectal compression trained using the compressed visual field. 708
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addition, Scott (18) reached a similar conclusion on the nature of a red/ green discrimination in fish with retinotectal compression. It may therefore be assumed that the red/green discrimination trained here was performed on a color basis in all our groups of fish, While demonstrating that color discrimination was possible throughout a compressed visual field, Scott’s work could not prove that the analysis of color was normal. Almost all retinal ganglion cells projecting to the tectum change their connections during retinotectal compression. If the ganglion cell fibers fail to reconnect to the appropriate tectal cells during reformation of the visual projection, abnormalities would occur in interpretation of visual information throughout the visual field. Our results may address this question of whether or not interpretation of color is normal after retinotectal compression. We demonstrated that interocular transfer of the color discrimination occurs at approximately normal levels both to and from a compressed visual field. This result demonstrates that the pathways mediating interocular transfer of this discrimination are still functional after retinotectal compression. In addition, these results demonstrate that interpretation of color information must be essentially the same in both the normal tectum and the tectum receiving a compressed visual projection. If this were not so, the discrimination presented to the different visual fields would appear to differ, abolishing the performance of the discrimination on interocular transfer. In view of the success of interocular transfer of the color discrimination, the transfer deficit seen in fish with unilateral retinotectal compression trained with the orientation discrimination on the normal visual field is initially surprising. However, Ingle (9) demonstrated that interocular transfer of a color discrimination occurs more easily than transfer of a pattern discrimination in normal fish, implying that different mechanisms of transfer operate in the two cases. Such a difference in mechanisms of transfer may explain the difference in effects of retinotectal compression on interocular transfer of the two discriminations seen here. Attempting to explain the small degree of interocular transfer of the orientation discrimination from the normal to the compressed visual field is difficult without more detailed knowledge of the mechanisms in learning and interocular transfer of the discrimination. The following points may, however, be raised. First, the failure of interocular transfer to the compressed visual field cannot be attributed to an inability of the fish to perform the discrimination using the compressed visual field. Though acquisition of the orientation discrimination on the compressed visual field was slower than normal, learning was shown to occur. Furthermore, it is unlikely that the small degree of discrimination on transfer may be attributed to differences in interpretation of the stimuli viewed by the normal and compressed visual
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fields. Such a difference ought to cause failure in transfer of the discrimination both to and from the compressed visual field. This reasoning implies that the failure lies within the mechanisms underlying interocular transfer. One immediately obvious factor that could affect interocular transfer is damage of the tectal commissure which inevitably accompanies caudal half-tectal ablation. It is known, however, that integrity of the tectal commissure is not necessary for interocular transfer of a classically conditioned horizontal/vertical discrimination (24). Only the postoptic commissures (which are not damaged by caudal tectal ablation) have been shown to be necessary for interocular transfer of a classically conditioned orientation discrimination (25). The most obvious (and best documented) effect of partial tectal ablation is a loss of original retinal connections to the tectum and their reformation in different loci on the tectum (i.e., compression of the visual projection). It is therefore tempting to suggest that this is responsible for the apparent deficits in interocular transfer. Previous studies indicate that the engram of a unilaterally learned visual discrimination is deposited in both halves of the brain under normal circumstances (7, 10, 25). This suggests the possibility that the retinal ganglion cell fibers displaced during compression of the visual projection may connect normally to the commissural systems mediating transfer of information to the opposite brain half, but fail to connect to the systems holding the engram transferred from the other half of the brain. In that case, information could be transferred normally to the intact tectum where the unaltered retinal connections could mediate use of the information. However, information transferred from the normal brain half could not be used by the compressed visual projection. This suggestion must be reconciled with the success of interocular transfer of a pattern discrimination after unilateral optic nerve crush and regeneration (3). This latter case represents a loss and reformation of original connections [with some decrease in the precision of connections ( 14)]. In the case of retinotectal compression, an entirely new set of connections are formed. It is possible that this difference is crucial in determining function. It should, however, be pointed out that alteration of retinal connections is not the only change that would be expected as a result of partial tectal ablation. After half-tectal ablation, the other loci of the brain that project to the tectum will be partially de-efferented. Similarly, systems receiving projections from the tectum will be partially denervated. Such a situation is likely to lead to a rearrangement of connections in these tectal afferent and efferent connections as was reported in the projection of the nucleus isthmi to the optic tectum (2). It is therefore likely that the systems mediating interocular transfer will also show changes in their connections. It may, therefore, be abnormalities in these connections that are responsible
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for the deficits in interocular transfer indicated by our results. Again, without understanding of the connections mediating interocular transfer, it is difficult to suggest why such abnormalities should lead to unilateral transfer deficits. Deficits were observed in the acquisition of the color discrimination when trained on a compressed visual field. It does not, however, seem necessary to hypothesize that these deficits represent more than a mass action effect as half-tectal ablation decreases the mass of tectal tissue available for the analysis of the visual stimuli. Our demonstration of poorer learning of an unstructured visual discrimination agrees with the results of Yolen and Hodos (26). Those authors reported results suggesting a slight deficit in the acquisition of a black/white discrimination after bilateral halftectal ablations. However, Yolen and Hodos’s results also indicate a much more dramatic deficit on the acquisition of a horizontal/vertical discrimination after bilateral retinotectal compression. Our results agree that deficits occur in the learning of an orientation discrimination on a compressed visual field, but the deficits that we observe do not appear much greater than the deficits seen when training a color discrimination. One factor that may have contributed to the magnitude of the learning deficit observed by Yolen and Hodos is their use of a bilateral training model. As discussed, our results indicate that interocular transfer of an orientation discrimination to a tectum receiving a compressed retinal projection is deficient. It therefore seems likely that transfer of information would be deficient after bilateral retinotectal compression and that this would affect transfer both to and from each half of the brain. In the absence of such transfer, both halves of the brain would effectively have to learn the discrimination separately. Thus, despite the fact that the task was trained bilaterally, it would effectively be learned unilaterally. In that case, the deficits associated with unilateral learning of a task (16) would be added to the direct effects of partial tectal ablation. This combination of effects might explain the sizeable learning deficits (relative to bilaterally taught controls) that Yolen and Hodos observed. Our subjects were compared against unilaterally taught controls and were themselves taught unilaterally. For this reason, the difference between controls and operated fish should not he so great. It remains possible, however, that some bilateral participation in learning occurs under normal circumstances with a unilaterally trained task [although Yeo (23) did not report such a deficit after blocking transfer of an orientation discrimination by postoptic commissure section]. If so, this may explain the slower acquisition of the orientation discrimination by fish with retinotectal compression trained on the normal visual field. Our results contrast with the statement by Yager (22) that no learning deficits were apparent when a fish was trained an orientation discrimination on a
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compressed visual field. Interpretation of this result is difficult because Yager did not give details of how he reached this conclusion. Furthermore, it is unclear from his paper whether he trained more than one subject. We have demonstrated in this paper that learning and unilateral interocular transfer of a structured discrimination is possible after unilateral retinotectal compression. In our next paper [of which a preliminary report has appeared (l)] we will describe experiments using these methods to compare visual angle analysis in normal and compressed visual fields. REFERENCES I. DUNN-MEYNELL, A. A., AND G. E. SAVAGE. 1982. Interocular transfer and visual angle analysis in goldfish with unilateral retinotectal compression. Sot. Neurosci. Absfr. 8: 453. 2. DUNN-MEYNELL, A. A., AND S. C. SHARMA. 1984. Changes in the topographically organized connections between the nucleus isthmi and the optic tectum after partial tectal ablations in adult goldfish. J. Camp. Neural. 227: 497-5 10. 3. FRANCIS, A., L. BENGSTON, AND M. S. GAZZANIGA. 1976. Interocular equivalence after optic nerve regeneration in goldfish. Exp. Neurol. 53: 94- 10 1. 4. GAZE, R. M., AND S. C. SHARMA. 1968. Axial differences in the reinnervation of the optic tectum by regenerating optic nerve fibres. J. Physiol. (London) 198: 117P. 5. GAZE, R. M., AND S. C. SHARMA. 1970. Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve Iibres. Exp. Bruin Rex 10: 171-18 I. 6. GELLERMAN, L. W. 1933. Chance orders of alternating stimuli in visual discrimination experiments. J. Genet. Psychol. 42: 206-208. 7. GREIF, K. F., AND M. Y. SCOTT. 1980. Interocular transfer of color discrimination after tectal lesions in goldfish. Exp. Neural. 67: 504-5 12. 8. HODOS, W., AND N. M. YOLEN. 1976. Behavioural correlates of “tectal compression” in goldfish. II. Visual acuity. Bruin Behav. Evol. 13: 468-474. 9. INGLE, D. J. 1965. Interocular transfer in goldfish: color easier than pattern. Science 149: 1000-1002. 10. INGLE, D. J. 1968. Interocular integration of visual learning by goldfish. Bruin Behav. Evol. 1: 58-85. 1 I. MCCLEARY, R. A., AND J. J. BERNSTEIN. 1959. A unique method for control of brightness cues in study of colour vision in fish. Physiol. Zool. 32: 284-292. 12. MEYER, R. L. 1977. Eye-in-water electrophysiological mapping of goldfish with and without tectal lesions. Exp. Neurol. 56: 23-41. 13. NORTHMORE, D. P. M. 1981. Visual localization after rearrangement of retinotectal maps in fish. Nature 293: 142-144. 14. NORTHMORE, D. P. M., AND T. MASINO. 1984. Recovery of vision after optic nerve crush: a behavioural and electrophysiological study. Exp. Neural. 84: 109- 125. 15. ROBERTS, M. G., D. E. WRIGHT, AND G. E. SAVAGE, 1973. A technique for obtaining the electrocardiogram of fish. Camp. B&hem. Phvsiol. 44: 665-668. 16. SCHULTE, A. 1957. Transfer und Transpositionsversuche mit monokular dressierten Fischen. Z. Vergl. Physiol. 39: 432-476. 17. SCOIT, M. Y. 1975. Functional capacity of compressed retinotectal projection in goldfish. Anal. Rec. 181: 474. 18. SCOTT, M. Y. 1976. Behavioral tests of compression of retinotectal projection after partial tectal ablation in goldfish. Exp. Neurol. 54: 579-590.
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19. SHARMA, S. C. 1972. The retinal projections in the goldfish: an experimental study. Bruin Res. 39: 213-223. 20. SIENKIEWICZ, 2. J. 1983. Lesions of the Nuckus Preglomerolulosus and Learning in Goldfish. Ph.D. Dissertation, University of London, England. 21. SPRINGER, A. D., AND J. S. GAFFNEY. 1981. Retinal projections in the goldfish: a study using cobaltous lysine. J. Comp. Neurol. 203: 401-424. 22. YAGER, D. 1978. Psychophysical functions in fish with respecified retinotectal connections. Pages 725-732 in S. J. COOL, AND E. L. SMITH, Eds., Frontiers in Visual Science. Springer, New York. 23. YEO, C. H. 1979. Interocular transfer in the goldfish. Pages 53-60 in I. S. RUSSEL, M. W. VAN HOF, AND G. BERLUCCHI, Eds. Structure and Function of Cerebral Commissures. Macmillan Press, London. 24. YEO, C. H., AND G. E. SAVAGE. 1975. The tectal commissure and interocular transfer of a shape discrimination in the goldfish. Exp. Neurol. 49: 291-298. 25. YEO, C. H., AND G. E. SAVAGE. 1976. Mesencephalic and diencephahc commissures and interocular transfer in the goldfish. Exp. Neurol. 53: 5 i-63. 26. YOLEN, N. M., AND W. HODOS. 1976. Bchavioural correlates of “tectal compression” in goldfish. I. Intensity and pattern discrimination. Brain Behav. Evol. 13: 45 l-467.
NEUROLOGY
I3 (1985)
88,696-7
Learning and Interocular Transfer of Visual Discriminations by Goldfish with Retinotectal Compression A.A.DuNN-MEYNELLANDG. Department
of Biology,
Queen
Mar?,
College,
Received
August
I. 1984; revision
E. SAVAGE'
Mile
End Road,
received
January
London,
England
El
4NS
28. 1985
Visual function mediated by a compressed retinotectal projection was examined by training goldfish with unilateral retinotectal compression to perform red/green and horizontal/vertical discriminations. Fish were trained monocularly via the compressed or the normal visual field using an aversive classical conditioning model. Interocular transfer was then examined to determine if the mechanisms mediating this transfer functioned normally after retinotectal compression and to compare interpretation of visual information via normal and compressed visual fields. Both visual discriminations were learned successfully using the normal or the compressed visual field. Learning deficits (relative to controls) were, however, observed in fish trained with the color discrimination using the compressed visual field. or the horizontal/vertical discrimination using the compressed or the normal visual field. Interocular transfer of the color discrimination from the compressed to the normal visual held or in the reverse direction was demonstrated to occur at approximately normal values. Interocular transfer of the horizontal/vertical discrimination was successful from the compressed to the normal visual field. but was reduced or absent in the opposite direction. The results indicate that analysis of the colors red and green is essentially normal after retinotectal compression, and that the pathways mediating interocular transfer of this color discrimination remain functional. There were, however, abnormalities in the mechanism mediating interocular transfer of pattern discriminations after retinotectal compression. 0 1985 Academic Press. Inc.
INTRODUCTION In teleost fish the vast majority in the optic tectum contralateral
of retinal ganglion cell fibers terminate to the eye of origin. This retinotectal
Abbreviations: DL-discrimination level, PD-percentage deceleration. i All correspondence should be sent to A.D.M. at his present address: Ophthalmology, New York Medical College, Valhalla, NY 10595.
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$3.00
Copynghl 0 1985 by Academic Press, Inc. All tights of reproduction in any form reserved.
Department
of
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projection is topographically ordered so that ganglion cells serving different areas of the visual field terminate at different positions in the tectum. The retinotectal projection is capable of showing a variety of forms of plasticity after surgical manipulation in adult fish. For example, if the caudal half of one tectum is removed, most or all of the ganglion cells previously projecting across the whole tectum come to project across the remaining half-tectum, a process known as retinotectal compression [see, for example, (4, 5, 12)]. Most studies of plasticity in the teleost visual system utilized electrophysiologic or anatomic techniques to examine the pattern of projection of ganglion cell fibers on the tectum. Little information is available with regard to changes in other portions of the central nervous system (including the tectal cells themselves) in response to changes in the retinotectal projection that follow tectal surgery. Our knowledge of whether or not altered retinal connections are capable of mediating normal perception and appropriate responses to visual stimuli is therefore relatively sparse. A few studies, however, have been conducted on the behavior of fish with compression of the visual field. Those studies demonstrated that the altered visual system is functional for guidance of motor activity (13) and for discrimination on the basis of orientation (8, 22, 26), color (17, 18), or intensity (26). In this paper we describe experiments that examined the ability of fish with unilateral retinotectal compression to perform interocular transfer of visual discriminations. Interocular transfer is the process by which learned responses to visual discriminations acquired using one eye may be demonstrated when stimuli are presented to the opposite eye. In goldfish, very few, if any retinal fibers project to the ipsilateral optic tectum (19, 2 1). Therefore, if a visual discrimination is presented in the monocular portion of one visual field, detailed visual information is relayed to only one half of the brain. For interocular transfer to occur, the visual information must be passed to the other brain half via the commissures linking the two sides of the brain. Francis et al. (3) showed that interocular transfer remained possible after regeneration of a crushed optic nerve. However, in experiments described in an unpublished manuscript, Campbell, Hope, and Ingle failed to demonstrate interocular transfer of pattern discriminations in fish with retinotectal compression. If this latter result proves correct, it would indicate a previously unsuspected abnormality in tectal connections after partial tectal ablation and visual field reorganization. Alternatively, if this observation were incorrect, interocular transfer in fish with unilateral retinotectal compression will provide an excellent system for comparison of the analysis of visual information between normal and compressed visual fields. In addition to examining the feasibility of interocular transfer, our experiments allow a reexamination of the effects of retinotectal compression on learning. Previous studies have been contradictory over whether or not
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partial tectal ablation and visual acquisition of visual discriminations
AND
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field compression (22, 26).
leads to deficits
in
METHODS The experiments were carried out on 7- to 1 l-cm goldfish (Curassius LZWU~US) which were kept under a 15-h light:9-h dark schedule at 17 to 21°C. Partial tectal ablations were carried out on each of 46 fish using the following methodology: The fish was anesthetized with MS222 solution which was then passed over the gills to maintain anesthesia. A flap of cranium was removed to reveal one tectal lobe. Using a sharpened tungsten needle, an incision about 300 /*rn deep was made in the tectum. The incision extended from the dorsomedial to the ventrolateral edge of the tectal lobe, splitting the tectum into rostra1 and caudal halves. The caudal half was then removed by aspiration. After this the cranial flap was glued back into place and the fish was revived. In each of a further 11 fish, sham operations were made. These fish were anesthetized and the cranium was opened as described, and then the cranium was resealed without tectal surgery and the animals were revived. All fish (including the sham-operated controls) were then left 3.5 to 22 months before further use. Maps of the retinotectal projection were made of 21 of the fish with partial tectal ablations (six of these fish were also trained with one of the visual discriminations) and of 15 unoperated controls. To map the projection, the fish was anesthetized, its cranium was opened, and the animal was positioned at the center of a visual perimeter. For each of a series of points on the optic tectum (Figs. 1 and 2), an extracellular electrode was lowered into the tectal lobe. Multicellular potentials were recorded with the electrode as a slowly flashing light was moved over the visual perimeter. The point at which the light elicited most activity was then noted, before the electrode was moved to the next tectal locus. The fish were trained using classical conditioning of their cardiac deceleratory response to aversive stimuli. The electrocardiogram (ECG) was recorded by electrodes implanted using the methods of Roberts et at. (15). Briefly, the fish was anesthetized and the scales were scraped from a small patch of skin on its ventral aspect between the pectoral fins. Electrodes were then implanted through the bared patch so that their tips lay adjacent to the pericardium, and were glued in place, before the fish was revived; 1 h for postoperative recovery elapsed before the start of training. After implantation of the electrodes, the fish was restrained in a plasticmesh envelope. Thus immobilized, the animal was placed in a T-shape black Perspex Chamber. The base of the T (in which the fish was held)
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measured 14 cm long X 3 cm wide X 6 cm deep. The front 4 cm of this chamber was open to the side arms which were 8 cm long X 4 cm wide X 6 cm deep. The animal was positioned so that the left eye had an unrestricted view into the left arm of the T and the right eye into the right arm. Neither eye could see into the arm on the opposite side. The visual stimuli were presented at the end of the side arms during training. An opaque cover was placed over the training chamber to prevent the fish from viewing the stimuli except when they were in place, or from seeing the experimenter. The chamber was suspended in a tank containing water at 19 to 2 1“C. The subject’s ECG was recorded with a Washington MD2 pen recorder and passed to a microprocessor that counted heart beats. The microprocessor also controlled trial onset and delivered shock reinforcement through a pair of copper plates adjacent to the fish’s tail. Each subject was trained to perform either a color (red/green) or an orientation (horizontal/vertical) discrimination. The stimuli used for training the color discrimination were 2-cm-diameter disks of plastic painted with Humbrol Emerald Green gloss paint, or Humbrol Brilliant Red gloss paint. The orientation discrimination was trained using 1.5- X 0.5-cm bars of white plastic mounted horizontally or vertically. All stimuli were mounted on the end of matt black wires. Three groups of fish were trained with each of the two discriminations: operated controls (cant); fish with retinotectal compression trained using the normal visual projection (RTC-norm) and fish with retinotectal compression trained with the compressed projection (RTC-camp). The color discrimination was trained to 5 controls, 5 fish with retinotectal compression trained with the normal visual field, and 6 fish trained with the compressed visual field. The orientation discrimination was trained to 6 controls, 7 fish with tectal surgery trained with the normal visual field, and 13 fish trained with the compressed field. Half an hour before commencing training, the subject was placed in the apparatus. Before training began, the AC electric shock was adjusted to an intensity sufficient to produce an unconditioned response of a cardiac deceleration of approximately 50% for 4 s after shock application. Each subject was trained monocularly using the same eye throughout habituation and training trials. In an individual trial, the number of heart beats was counted for 10 s, and then one of the stimuli was presented at the end of one side arm for 10 s, while the heart beats were again counted. During presentation, the stimulus was bobbed up and down through approximately 2 cm at one up-down cycle per second. At the end of the presentation period, before the stimulus was removed from the side arm, a 0.5-s electric shock was delivered if appropriate. Trials were given every 120 + 30 s. Each fish was trained in a single session of 130 trials. Training began
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with 20 habituation trials during which no electric shocks were given. During these habituation trials, as well as throughout the training trials, the stimulus order followed a semirandom, Gellerman sequence (6). After the habituation trials, the stimulus that had elicited least unconditioned cardiac deceleration was designated reinforced (+) and was followed by shock during the training trials. The other stimulus was designated unreinforced (-) and was not followed by shock. One hundred training trials were then given, followed by 10 unreinforced transfer trials with the stimuli presented to the naive eye. During the transfer trials the stimuli were presented in the sequence -++--++--+. During training, the conditioning results were analysed by the microprocessor as follows: For each trial, the number of heart beats during the 10 s before stimulus presentation (PRE) and the number of heart beats occurring during the 10-s presentation period (DUR) were counted. The percentage deceleration of the heart rate in response to the stimulus (PD) was then calculated as: PD = ((PRE - DUR)/PRE) X 100%. A positive value for this measure indicated a deceleration of the heart and a negative value indicated the opposite. To quantify the subject’s performance of the discrimination between the two stimuli, the discrimination level (DL) was calculated. The data were divided into 10 trial blocks. For each block, the average percentage decelerations in response to the stimulus that was reinforced during the training trials (PD+) and in response to the negative stimulus (PD-) were calculated. The DL was then derived for each IO-trial block using the following equation: DL = ((PD+ - PD-)/(PD+ + PD-)) X 100%. A positive DL indicated that the subject responded more to the reinforced stimulus than to the unreinforced one, and a negative DL indicated the reverse. Because the above equation yielded meaningful results only when PD- and PD+ were positive, an arbitrary DL was assigned when negative PDs occurred (that is, when the heart rate increased in response to the stimulus, a very rare event). If both PD- and PD+ were negative, then a DL of zero was assigned for that lo-trial block. If only PD’ was negative, the greatest negative DL observed in that animal prior to the IO-trial block concerned was assigned (or zero if no negative DL had been observed). Similarly, the greatest positive DL or zero was assigned if only PD- was negative. To quantify the rate of acquisition of the discrimination, a trials-tocriterion measure was calculated. The criterion level for each of the two tasks was set as one-half the overall average DL for the last 50 training trials in the control group trained with the corresponding task. This gave a DL of 2 1.1% for the color discrimination and 13.1% for the orientation discrimination. Moving averages were then calculated for the training data of each animal, averaging three IO-trial blocks. The first trio of IO-trial
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blocks in which the average DL exceeded the criterion DL was taken as the point at which criterion was attained, and the trials to criterion was set for that animal as the last trial in those three blocks. Thus if the DLs that a subject gave in the first, second, and third lo-trial blocks after training began were greater than the criterion level when averaged together, 30 trials to criterion was recorded. If not, the DLs of the second, third, and fourth lo-trial blocks were averaged and 40 trials to criterion was recorded if the criterion was attained. If criterion was not attained during the 100 training trials, 110 trials to criterion was arbitrarily assigned. RESULTS Evidence of visual field compression was seen in all retinotectal maps of fish with partial tectal ablations. Examples of normal and compressed retinotectal maps are shown in Fig. 1 and 2, respectively. The results from animals trained with the color discrimination are described first. Table 1 shows the average percentage decelerations in response to the reinforced and unreinforced stimuli. These figures are for each of the three treatment groups and for each lo-trial block. Because evidence of learning was biased against by the selection of the stimulus eliciting least unconditioned response during habituation as the reinforced stimulus, DL values significantly above zero demonstrated that learning had occurred. To yield a single measure of the degree of discrimination displayed by each animal by the end of training, the DLs from the last three lo-trial blocks before testing for interocular transfer were averaged for each subject. This average was termed the DLtrain. The DLtrains of each group of fish were statistically tested to determine if they were significantly above zero. One-tailed Wilcoxon matched-pair signed ranks tests were used for this purpose (for this test the DLtrain was treated as the difference between a matched pair of observations, the relative response to reinforced and unreinforced stimuli). These tests showed that all groups had DLtrains significantly above zero and had therefore learnt the discrimination (Cont: N = 5; T = 0; P < 0.05. RTC-norm: N = 5; T = 0; P < 0.05. RTC-camp: N = 6; T = 0; P < 0.025). The average DLtrains f SE for the animals trained with the color discrimination are shown in Fig. 3. The DLtrains of the control fish were compared with the fish in the other two groups using one-tailed Wilcoxon rank sum tests. These tests showed that neither of the experimental groups had DLtrains significantly lower than the controls (RTC-norm: M = 5; N = 5; T = 24.5; P > 0.05. RTC-camp: A4 = 5; N = 6; T = 35; P > 0.05). The trials-to-criterion results for fish trained with the color discrimination are shown in Fig. 4. The fish with unilateral retinotectal compression
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IWFElllOll
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FIG. I. The retinotectal map of a control fish. At the top of the figure is shown a representation of the subject’s left visual field. Below is a diagram of the dorsal surface of the right tectal lobe. Nervous activity was recorded from an electrode lowered into each of the loci indicated on the tectal diagram by numbers. The numbers in the visual field diagram indicate the positions at which a visual stimulus elicited maximum response recorded at the correspondingly numbered electrode positions. Electrode positions running rostrocaudally along the tectum and their corresponding visual field positions are joined by lines to ease interpretation of the diagram. The edge of the visual field diagram extends I IO” from its center.
trained by the normal visual field learned slightly more slowly than the controls; however, the difference in trials to criterion was not significant (A4 = 5, N = 5, T = 30, P > 0.05). The fish trained by the compressed visual field, however, required a significantly greater number of trials to criterion than did the controls (A4 = 5, N = 6, T = 19, P < 0.025). These significances were calculated using one-tailed Wilcoxon rank sum tests. In both groups with retinotectal compression, the average DL during the interocular transfer trials (DLtransfer) was significantly above zero (calculated
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LEFT
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FIG. 2. The retinotectal map of a fish with a compressed visual field. The shaded portion of tectum had been ablated.
using one-tailed Wilcoxon matched-pairs signed rank tests; RTC-norm: M = 5; T = 0; P < 0.05. RTC-camp: A4 = 6; T = 2; P < 0.05). This demonstrated the success of interocular transfer in the two experimental groups. Due to equipment malfunction, the interocular transfer data were lost from one control animal. Consequently a Wilcoxon matched-pairs signed ranks test could not be used here (because this test cannot prove significance at the 0.05 level with less than five values). However, the DLtransfer of the controls was well above zero (Fig. 3) and the standard error was relatively small, strongly implying that transfer was also successful in this group. In evaluating the degree of interocular transfer it is of little value to compare directly the DLtransfer levels of groups that attained different levels of discrimination at the end of training. A more meaningful measure is the ratio of discrimination level during the transfer trials relative to the
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Average
Percentage
1 2 3 4 5 6 7 8 9 10 11 12 13
1
Decelerations in Response to Reinforced and Unreinforced by Fish Trained with the Color Discrimination” Cont
1O-Trial block
SAVAGE
RTC-norm
RTC-camp
Unreinforced
Reinforced
Unreinforced
Reinforced
Unreinforced
23.5 20.7 8.9 6.1 18.2 29.6 29.6 25.2 20.1 18.4 14.4 9.8 15.7
21.4 10.0 6.5 21.6 30.0 43.3 43.6 47.5 39.4 33.7 38.2 34.0 37.4
35.9 10.2 8.9? 30.6 26.7 27.2 29.3 32.8 24.7 24.2 20.9 21.0 27.6
26.0 10.2 23.7* 43.2 46.0 52.3 54.9 57.8 62.2 63.3 62.7 57.9 48.4
40.2 26.5 21.2? 13.9 24.0 38.3 31.0 41.8 37.5 28.4 37.0 32.3 32.5
f 8.4 + 8.9 f 8.2 f 5.6 + 6.8 k 11.7 + 10.8 + 8.3 + 11.3 + 8.1 ? 7.0 k 4.0 k 4.3
f f 2 f + + f f + f + f -c
4.1 10.2 2.6 5.8 12.3 16.6 14.3 11.1 12.1 9.6 12.9 9.3 9.7
f f f f f k + + + + + +
4.3 4.1 5.2 8.7 9.0 9.7 10.0 9.8 8.4 7.9 9.7 9.7 9.2
Stimuli
f f + k + + f + f + f +
3.2 4.9 5.1 10.0 10.6 11.4 11.9 6.8 7.1 6.0 8.7 10.7 8.6
f 7.4 +- 8.6 7.6 f 4.9 + 7.1 f 11.2 f 11.2 f 10.6 f 8.6 f 5.9 f 7.5 f 8.4 f 4.6
Reinforced 40.5 10.5 19.1 14.7 32.7 45.0 42.5 50.4 57.3 59.1 54.3 59.1 47.4
f f f f f f f + f + -t f k
7.2 6.4 10.1 13.5 9.6 14.0 14.3 12.2 10.4 7.2 7.7 6.2 7.0
’ For each animal, the responses to the stimulus that was reinforced during training and to the negative stimulus were averaged within each lo-trial block. These values were then used to calculate the mean responses to the two stimuli f SE for each experimental group in each lotrial block. The first two lo-trial blocks were the habituation trials. the next 10 blocks were the training trials, and the last block was the transfer trials. Cont-controls. RTC-norm-fish with unilateral retinotectal compression trained on the normal visual field and tested for interocular transfer using the compressed visual field. RTC-camp-fish trained on the compressed visual field and tested for interocular transfer using the normal visual field.
level at the end of training, i.e., (DLtransfer/DLtrain) X 100%. Such a measure was used by Yeo and Savage (24) and termed the “transfer level.” A transfer level of 100% indicates that the discrimination was performed equally well before and after transfer. A transfer level of 0% would indicate a complete failure of interocular transfer (equal response to both stimuli on transfer testing). The three groups trained with the color discrimination attained the following transfer level (X + SE): cant, 81.5 + 28.9%; RTC-norm, 62.2 + 8.7%; RTC-camp, 69.7 + 47.3%. Thus the two groups with retinotectal compression showed transfer level similar to, though slightly lower than that observed in controls. The difference in transfer levels between the controls and the fish with retinotectal compression were not statistically significant (calculated using two-tailed Wilcoxon rank sum tests: RTC-
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tr.,n RTC-norm
RTC-camp
FIG. 3. The group average discrimination levels + SE during the last 30 training trials (train) and during the transfer trials (trans) for the three groups trained with the color discrimination. Con&controls. RTC-norm-animals with unilateral retinotectal compression trained on the normal visual field and tested for interocular transfer on the compressed visual field. RTCcamp-fish with retinotectal compression trained on the compressed visual field and tested for interocular transfer on the normal visual field.
norm: M = 4; N = 5; T = 2 1; P > 0.05. RTC-camp:
M = 4; N = 6; T
= 27; P > 0.05). A similar set of analyses was carried out on the data obtained from fish trained with the horizontal/vertical discrimination. The average percentage decelerations in response to the two stimuli are shown in Table 2. Subjects in all three groups successfully acquired the orientation discrimination. This was demonstrated by the DLtrains of the subjects in each group (shown in Fig. 5) which were significantly above zero (cant: N = 6; T = 0; P < 0.025. RTC-norm: N = 7; T = 0; P c 0.0025. RTC-comp: N = 13; T = 5; P < 0.005). The group of fish with retinotectal compression trained on the compressed visual field attained a significantly lower DLtrain than the controls (M = 6, N = 13, T = 79, P = 0.05). The animals with retinotectal compression trained on the normal visual field did not differ significantly in DLtrain from the controls (M = 6, N = 7, T = 42, P > 0.05). The trialsto-criterion measure, however, showed that both groups with retinotectal compression learned significantly more slowly than the controls (RTC-
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= ; 0 0 c
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M
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: (E c
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2010-
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RTCcamp
FIG. 4. The group average trials to criterion 2 SE for the three groups trained with the color discrimination. Cont-controls. RTC-norm-animals with retinotectal compression trained on the normal visual field. RTC-comp-fish with retinotectal compression trained on the compressed visual field.
norm: A4 = 6; N = 7; T = 27.5; P < 0.025. RTC-camp: M = 6; N = 13: T = 3 1; P = 0.005). The group average trials-to-criterion and SE are shown in Fig. 6. Both the controls and the animals with retinotectal compression trained on the compressed visual field were demonstrated to show interocular transfer of the visual discrimination as their DLtransfers were significantly above zero (cant: N = 6; T = 0; P < 0.025. RTC-camp: N = 13; T = 15.5; P < 0.025). However, the average DLtransfers of the fish with retinotectal compression trained on the normal visual field were not significantly above zero (N = 7, T = 14, P > 0.05). The average transfer levels confirmed that transfer was successful in controls (transfer level 72.2 k 24.9%) and in fish with retinotectal compression trained on the operated tectum (113.4 + 73.5%). The transfer levels of the fish in these two groups did not differ significantly (M = 6, N = 13, T = 58, P > 0.1). The transfer level of the fish with retinotectal compression trained on the normal visual field and tested for interocular transfer on the compressed visual field was, however, slightly below zero (-5.9 + 20.1%) suggesting a complete failure of interocular transfer. The difference in transfer levels between fish in this group and the controls was statistically significant (M = 6, N = 7, T = 56, P < 0.05).
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TABLE 2 Average Percentage Decelerations in Response to Reinforced and Unreinforced Stimuli by Fish Trained with the Horizontal/Vertical Color Discrimination” Cont 1O-Trial block 1 2 3 4 5 6 7 8 9 10 11 12 13
Unreinforced 16.4 + 8.1 + -6.6 k 19.3 f 27.4 f 25.7 + 23.8 f 31.0 f 40.3 f 37.5 f 40.7* 32.4 f 29.4 +
7.8 3.8 7.1 3.1 4.3 3.1 5.0 6.2 7.8 8.4 6.5 5.1 6.0
RTC-norm
RTC-camp
Reinforced
Unreinforced
Reinforced
16.5 f 5.6 6.0 + 3.7 3.6 f 7.3 24.7k4.0 33.8 + 3.8 34.6 f 3.9 33.6 + 4.2 48.3 + 8.0 55.4 + 7.2 60.0 f 8.0 58.6 + 5.7 63.1 + 6.0 41.3 + 9.4
27.1 + 6.9 13.9 I~I 5.6 5.3 f 5.2 11.3? 4.1 21.3 f 7.1 41.6 + 10.0 41.5 + 9.8 39.4 + 9.4 38.1 + 8.2 29.2 + 8.2 37.8 + 6.9 29.3 f 7.1 35.7 f 7.8
20.0 4.3 8.2 7.7 13.9 43.5 38.9 47.9 44.1 45.3 55.9 52.5 37.3
+ + f + + f f + f + f f +
6.0 8.1 2.9 5.0 8.0 11.9 8.4 8.4 8.8 9.7 8.6 7.7 7.1
Unreinforced 26.1 25.6 16.2 24.1 30.5 33.1 34.8 33.3 38.8 38.5 35.8 39.3 36.1
+ + f + + + + + + + + + +
5.2 5.1 5.2 4.7 4.9 5.1 4.7 4.3 5.0 4.6 5.6 4.8 4.4
Reinforced 19.8 21.0 15.7 25.6 32.1 36.6 38.5 43.9 41.7 48.3 46.4 54.3 46.0
f f f f f f f f f f + f f
5.5 5.1 5.0 3.7 5.0 6.5 5.7 5.8 6.7 6.0 6.9 6.7 4.9
a Calculations were performed as described for Table 1. Cont-controls. RTC-norm-fish with unilateral retinotectal compression trained using the normal visual field and tested for interocular transfer via the compressed visual projection. RTC-comp-fish with retinotectal compression trained by the compressed field and tested via the normal field.
DISCUSSION Our results confirm that color and horizontal/vertical discriminations may be learned by goldfish with unilateral retinotectal compression on the normal or the compressed visual field. We demonstrate, however, that deficits occur in the acquisition of either discrimination on the compressed visual field and of the orientation discrimination on the normal visual field. We also show that interocular transfer of the color discrimination is possible both to and from the brain half with retinotec@ compression. However, interocular transfer of the orientation discrimination could be proven only from the compressed to the normal visual projection. Our demonstration that a red/green discrimination may be learned on a compressed visual field confirms Scott’s finding (17, 18). Previous studies have shown that normal goldfish learn a red/green discrimination on a color rather than an intensity basis. This was originally demonstrated by McCleary and Bernstein (11) and was confirmed by Sienkiewicz (20). Sienkiewicz presented the stimuli in the same manner as we employed and his training stimuli were colored identically to those that we used. In
35
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J
train
trans
RTC-norm trans train
!!!
RTC-camp tran* train
FIG. 5. The average discrimination levels + SE for the last 30 training trials (train) and for the transfer trials (trans) in the groups trained to perform the orientation discrimination. Cont-controls. RTC-norm-fish with retinotectal compression trained using the normal visual field and tested for interocular transfer on the compressed visual field. RTC-camp-fish with retinotectal compression trained using the compressed visual field and tested for interocular transfer on the normal visual field.
90
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0 c a : ; c
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50 40 30 20
norm CObVlP FIG. 6. Group average trials to criterion + SE for the groups trained with an orientation discrimination. Cont-controls. RTC-norm-animals with retinotectal compression trained using the normal visual field. RTC-camp-fish with retinotectal compression trained using the compressed visual field. 708
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addition, Scott (18) reached a similar conclusion on the nature of a red/ green discrimination in fish with retinotectal compression. It may therefore be assumed that the red/green discrimination trained here was performed on a color basis in all our groups of fish, While demonstrating that color discrimination was possible throughout a compressed visual field, Scott’s work could not prove that the analysis of color was normal. Almost all retinal ganglion cells projecting to the tectum change their connections during retinotectal compression. If the ganglion cell fibers fail to reconnect to the appropriate tectal cells during reformation of the visual projection, abnormalities would occur in interpretation of visual information throughout the visual field. Our results may address this question of whether or not interpretation of color is normal after retinotectal compression. We demonstrated that interocular transfer of the color discrimination occurs at approximately normal levels both to and from a compressed visual field. This result demonstrates that the pathways mediating interocular transfer of this discrimination are still functional after retinotectal compression. In addition, these results demonstrate that interpretation of color information must be essentially the same in both the normal tectum and the tectum receiving a compressed visual projection. If this were not so, the discrimination presented to the different visual fields would appear to differ, abolishing the performance of the discrimination on interocular transfer. In view of the success of interocular transfer of the color discrimination, the transfer deficit seen in fish with unilateral retinotectal compression trained with the orientation discrimination on the normal visual field is initially surprising. However, Ingle (9) demonstrated that interocular transfer of a color discrimination occurs more easily than transfer of a pattern discrimination in normal fish, implying that different mechanisms of transfer operate in the two cases. Such a difference in mechanisms of transfer may explain the difference in effects of retinotectal compression on interocular transfer of the two discriminations seen here. Attempting to explain the small degree of interocular transfer of the orientation discrimination from the normal to the compressed visual field is difficult without more detailed knowledge of the mechanisms in learning and interocular transfer of the discrimination. The following points may, however, be raised. First, the failure of interocular transfer to the compressed visual field cannot be attributed to an inability of the fish to perform the discrimination using the compressed visual field. Though acquisition of the orientation discrimination on the compressed visual field was slower than normal, learning was shown to occur. Furthermore, it is unlikely that the small degree of discrimination on transfer may be attributed to differences in interpretation of the stimuli viewed by the normal and compressed visual
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fields. Such a difference ought to cause failure in transfer of the discrimination both to and from the compressed visual field. This reasoning implies that the failure lies within the mechanisms underlying interocular transfer. One immediately obvious factor that could affect interocular transfer is damage of the tectal commissure which inevitably accompanies caudal half-tectal ablation. It is known, however, that integrity of the tectal commissure is not necessary for interocular transfer of a classically conditioned horizontal/vertical discrimination (24). Only the postoptic commissures (which are not damaged by caudal tectal ablation) have been shown to be necessary for interocular transfer of a classically conditioned orientation discrimination (25). The most obvious (and best documented) effect of partial tectal ablation is a loss of original retinal connections to the tectum and their reformation in different loci on the tectum (i.e., compression of the visual projection). It is therefore tempting to suggest that this is responsible for the apparent deficits in interocular transfer. Previous studies indicate that the engram of a unilaterally learned visual discrimination is deposited in both halves of the brain under normal circumstances (7, 10, 25). This suggests the possibility that the retinal ganglion cell fibers displaced during compression of the visual projection may connect normally to the commissural systems mediating transfer of information to the opposite brain half, but fail to connect to the systems holding the engram transferred from the other half of the brain. In that case, information could be transferred normally to the intact tectum where the unaltered retinal connections could mediate use of the information. However, information transferred from the normal brain half could not be used by the compressed visual projection. This suggestion must be reconciled with the success of interocular transfer of a pattern discrimination after unilateral optic nerve crush and regeneration (3). This latter case represents a loss and reformation of original connections [with some decrease in the precision of connections ( 14)]. In the case of retinotectal compression, an entirely new set of connections are formed. It is possible that this difference is crucial in determining function. It should, however, be pointed out that alteration of retinal connections is not the only change that would be expected as a result of partial tectal ablation. After half-tectal ablation, the other loci of the brain that project to the tectum will be partially de-efferented. Similarly, systems receiving projections from the tectum will be partially denervated. Such a situation is likely to lead to a rearrangement of connections in these tectal afferent and efferent connections as was reported in the projection of the nucleus isthmi to the optic tectum (2). It is therefore likely that the systems mediating interocular transfer will also show changes in their connections. It may, therefore, be abnormalities in these connections that are responsible
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for the deficits in interocular transfer indicated by our results. Again, without understanding of the connections mediating interocular transfer, it is difficult to suggest why such abnormalities should lead to unilateral transfer deficits. Deficits were observed in the acquisition of the color discrimination when trained on a compressed visual field. It does not, however, seem necessary to hypothesize that these deficits represent more than a mass action effect as half-tectal ablation decreases the mass of tectal tissue available for the analysis of the visual stimuli. Our demonstration of poorer learning of an unstructured visual discrimination agrees with the results of Yolen and Hodos (26). Those authors reported results suggesting a slight deficit in the acquisition of a black/white discrimination after bilateral halftectal ablations. However, Yolen and Hodos’s results also indicate a much more dramatic deficit on the acquisition of a horizontal/vertical discrimination after bilateral retinotectal compression. Our results agree that deficits occur in the learning of an orientation discrimination on a compressed visual field, but the deficits that we observe do not appear much greater than the deficits seen when training a color discrimination. One factor that may have contributed to the magnitude of the learning deficit observed by Yolen and Hodos is their use of a bilateral training model. As discussed, our results indicate that interocular transfer of an orientation discrimination to a tectum receiving a compressed retinal projection is deficient. It therefore seems likely that transfer of information would be deficient after bilateral retinotectal compression and that this would affect transfer both to and from each half of the brain. In the absence of such transfer, both halves of the brain would effectively have to learn the discrimination separately. Thus, despite the fact that the task was trained bilaterally, it would effectively be learned unilaterally. In that case, the deficits associated with unilateral learning of a task (16) would be added to the direct effects of partial tectal ablation. This combination of effects might explain the sizeable learning deficits (relative to bilaterally taught controls) that Yolen and Hodos observed. Our subjects were compared against unilaterally taught controls and were themselves taught unilaterally. For this reason, the difference between controls and operated fish should not he so great. It remains possible, however, that some bilateral participation in learning occurs under normal circumstances with a unilaterally trained task [although Yeo (23) did not report such a deficit after blocking transfer of an orientation discrimination by postoptic commissure section]. If so, this may explain the slower acquisition of the orientation discrimination by fish with retinotectal compression trained on the normal visual field. Our results contrast with the statement by Yager (22) that no learning deficits were apparent when a fish was trained an orientation discrimination on a
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compressed visual field. Interpretation of this result is difficult because Yager did not give details of how he reached this conclusion. Furthermore, it is unclear from his paper whether he trained more than one subject. We have demonstrated in this paper that learning and unilateral interocular transfer of a structured discrimination is possible after unilateral retinotectal compression. In our next paper [of which a preliminary report has appeared (l)] we will describe experiments using these methods to compare visual angle analysis in normal and compressed visual fields. REFERENCES I. DUNN-MEYNELL, A. A., AND G. E. SAVAGE. 1982. Interocular transfer and visual angle analysis in goldfish with unilateral retinotectal compression. Sot. Neurosci. Absfr. 8: 453. 2. DUNN-MEYNELL, A. A., AND S. C. SHARMA. 1984. Changes in the topographically organized connections between the nucleus isthmi and the optic tectum after partial tectal ablations in adult goldfish. J. Camp. Neural. 227: 497-5 10. 3. FRANCIS, A., L. BENGSTON, AND M. S. GAZZANIGA. 1976. Interocular equivalence after optic nerve regeneration in goldfish. Exp. Neurol. 53: 94- 10 1. 4. GAZE, R. M., AND S. C. SHARMA. 1968. Axial differences in the reinnervation of the optic tectum by regenerating optic nerve fibres. J. Physiol. (London) 198: 117P. 5. GAZE, R. M., AND S. C. SHARMA. 1970. Axial differences in the reinnervation of the goldfish optic tectum by regenerating optic nerve Iibres. Exp. Bruin Rex 10: 171-18 I. 6. GELLERMAN, L. W. 1933. Chance orders of alternating stimuli in visual discrimination experiments. J. Genet. Psychol. 42: 206-208. 7. GREIF, K. F., AND M. Y. SCOTT. 1980. Interocular transfer of color discrimination after tectal lesions in goldfish. Exp. Neural. 67: 504-5 12. 8. HODOS, W., AND N. M. YOLEN. 1976. Behavioural correlates of “tectal compression” in goldfish. II. Visual acuity. Bruin Behav. Evol. 13: 468-474. 9. INGLE, D. J. 1965. Interocular transfer in goldfish: color easier than pattern. Science 149: 1000-1002. 10. INGLE, D. J. 1968. Interocular integration of visual learning by goldfish. Bruin Behav. Evol. 1: 58-85. 1 I. MCCLEARY, R. A., AND J. J. BERNSTEIN. 1959. A unique method for control of brightness cues in study of colour vision in fish. Physiol. Zool. 32: 284-292. 12. MEYER, R. L. 1977. Eye-in-water electrophysiological mapping of goldfish with and without tectal lesions. Exp. Neurol. 56: 23-41. 13. NORTHMORE, D. P. M. 1981. Visual localization after rearrangement of retinotectal maps in fish. Nature 293: 142-144. 14. NORTHMORE, D. P. M., AND T. MASINO. 1984. Recovery of vision after optic nerve crush: a behavioural and electrophysiological study. Exp. Neural. 84: 109- 125. 15. ROBERTS, M. G., D. E. WRIGHT, AND G. E. SAVAGE, 1973. A technique for obtaining the electrocardiogram of fish. Camp. B&hem. Phvsiol. 44: 665-668. 16. SCHULTE, A. 1957. Transfer und Transpositionsversuche mit monokular dressierten Fischen. Z. Vergl. Physiol. 39: 432-476. 17. SCOIT, M. Y. 1975. Functional capacity of compressed retinotectal projection in goldfish. Anal. Rec. 181: 474. 18. SCOTT, M. Y. 1976. Behavioral tests of compression of retinotectal projection after partial tectal ablation in goldfish. Exp. Neurol. 54: 579-590.
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19. SHARMA, S. C. 1972. The retinal projections in the goldfish: an experimental study. Bruin Res. 39: 213-223. 20. SIENKIEWICZ, 2. J. 1983. Lesions of the Nuckus Preglomerolulosus and Learning in Goldfish. Ph.D. Dissertation, University of London, England. 21. SPRINGER, A. D., AND J. S. GAFFNEY. 1981. Retinal projections in the goldfish: a study using cobaltous lysine. J. Comp. Neurol. 203: 401-424. 22. YAGER, D. 1978. Psychophysical functions in fish with respecified retinotectal connections. Pages 725-732 in S. J. COOL, AND E. L. SMITH, Eds., Frontiers in Visual Science. Springer, New York. 23. YEO, C. H. 1979. Interocular transfer in the goldfish. Pages 53-60 in I. S. RUSSEL, M. W. VAN HOF, AND G. BERLUCCHI, Eds. Structure and Function of Cerebral Commissures. Macmillan Press, London. 24. YEO, C. H., AND G. E. SAVAGE. 1975. The tectal commissure and interocular transfer of a shape discrimination in the goldfish. Exp. Neurol. 49: 291-298. 25. YEO, C. H., AND G. E. SAVAGE. 1976. Mesencephalic and diencephahc commissures and interocular transfer in the goldfish. Exp. Neurol. 53: 5 i-63. 26. YOLEN, N. M., AND W. HODOS. 1976. Bchavioural correlates of “tectal compression” in goldfish. I. Intensity and pattern discrimination. Brain Behav. Evol. 13: 45 l-467.