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Visual discrimination after bilateral removal of the visual cortex in the rabbit
Behavioural Brain Research, 9 (1983) 257-262
257
Elsevier Short Communication Visual discrimination after bilateral removal of the visual cortex in the rabbit
M.W. VAN HOF, J. VAN HOF-VAN DUIN and J.F. HOBBELEN Erasmus Universiteit Rotterdam, Dept. of Physiology I, P.O. Box 1738, Rotterdam (The Netherlands)
(Received February 3rd, 1983) (Revised version received March 15th, 1983) (Accepted April 18th, 1983) Key words: visual discrimination - visual cortex - rabbit
Rabbits were trained on a brightness and a vertical vs horizontal discrimination. After bilateral removal of the visual cortex the threshold of brightness discrimination was significantly higher. In addition, there was a severe impairment of striated pattern discrimination. After bilateral removal of the visual cortex in the rabbit, striated pattern discrimination learning is severely impaired, whilst brightness discrimination learning remains unaffected [6]. Recently, these results were confirmed in a study on two-stage removal of the visual cortex [1]. At the present time a further analysis of the nature of the behavioural deficit after bilateral removal of the visual cortex is in progress in our laboratory. M a n y years ago Lashley [4] described that the threshold of brightness discrimination was considerably lower in normal rats than in rats in which the visual cortex had been removed. The present paper deals with a similar study in the rabbit. Brightness discrimination thresholds were studied quantitatively before and after removal of the visual cortex in the rabbit. From previous experience we knew that in the rabbit bilateral removal of the visual cortex has an unacceptably high postoperative mortality rate. Therefore a two-stage surgical procedure was followed. The pattern discrimination apparatus and the shaping procedure have been described elsewhere [8, 9, 10]. Sixteen Dutch belted rabbits went through the training procedure illustrated in Figs. 1 and 2. The sequence of the training days is plotted on the x-axis, the percentage of correct choices on the y-axis. Throughout training 100 trials were given per day. The procedure started with a brightness discrimination. The brightness ratio between the rewarded and the unrewarded pattern was 100 : 1. The diameter of the targets was 10 cm. After the 90~o correct criterion had been reached on 2 consecutive days training was continued with vertical vs horizontal striations. The diameter of the patterns was 10 cm, the width of the black and white striations, 1.25 cm. After the 90~o 0166-4328/83/$03.00 ~c" 1983 Elsevier Science Publishers B.V.
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Fig. 1. Example of training procedure in one animal. On the y-axis the percentage of correct choices, on the x-axis the sequence of the days. All animals received 100 trials per day. The procedure started with a brightness discrimination (brightness ratio 100: 1). In all cases the brightest target was rewarded. After the 90,°,0 correct criterion had been reached on 2 consecutive days training was continued with vertical vs horizontal striations. The vertical striations were rewarded. After the 90% criterion had been reached on 2 consecutive days training was continued with various brightness ratios. Fifty trials of the original 100:1 brightness ratio randomly mixed with 50 trials of asmaller brightness ratio were given each day. At first this smaller brightness ratio was 100 : 13. This 100:13 ratio was given for 5 days or less, depending on whether the 90% correct criterion had been reached on 2 consecutive days. Thereafter smaller brightness ratios were used. The second half of the procedure is shown in Fig. 2.
o_ 0
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Fig. 2. The continuation of the training procedure shown in Fig. 1.
criterion had been reached on 2 consecutive days training was resumed on the brightness discrimination but with smaller brightness ratios. Fifty trials of the original 100:1 brightness ratio, randomly mixed with 50 trials of a smaller brightness ratio, were given each day. In all cases the brightest target had a luminance of 0.04 cd per c m 2. The brightest target was always rewarded and placed randomly left or right. As Figs. 1 and 2 show, each of the smaller brightness ratios (100 : 13, 16, 20, 25, 32, 40, 50, 63 and 80) was given for 5 days or less, depending on whether the 90~o correct criterion had been reached on 2 consecutive days. In all animals the percentage of correct choices
259 ©O
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Fig. 3. Discrimination with vertical vs horizontal striations before and after bilateral removal of the visual cortex.
with the 100 : 1 brightness ratio remained above the 90% correct level. Since these trials and the ones with the smaller brightness ratios were randomly mixed during the whole procedure it is unlikely that the breakdown of discrimination with the smaller brightness ratios was due to the fact that the animals ignored the patterns. All animals reached the 90~o correct criterion with the initial 100:1 brightness ratio with an average score of 375 (S.E. + 40.3) trials and 91.6 (S.E. + 12.0) errors to criterion. With vertical vs horizontal striations this criterion was reached after 331.3 (S.E. + 32.6) trials, errors to criterion 88.1 (S.E. + 12.1). In Fig, 4, the average percentage of correct choices on the last 2 days of all brightness ratios smaller than 100 : 1 are plotted. In every animal the brightness ratio corresponding with the 75 % correct choices was determined by means of a linear interpolation method [ 11]. The average of these values was 100:59.3 (S.E. + 2.31). After the training procedure was finished a cortical region including the
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8
16
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25
20
40
32
63
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Fig. 4. Percentage of correct choices on the y-axis, brightness ratio decreasing from 100' 1 to 100 : 80 on the x-axis.
260 visual cortex [3] and extending beyond V. ! and V.2 [3] was removed unilaterally by means of suction [7]. Three months later the other visual cortex was removed. After a recuperation period of 6 weeks, training was started again. All animals relearned the 100 : 1 brightness discrimination. Criterion was reached with an average score of 287.5 (S.E. _ 43.7) trials and 54.0 (S.E. _ 12.2) errors. Training was continued with vertical vs horizontal striations for 15 days. None of the animals reached the 90 ~o criterion. In Fig. 3, the average scores obtained with vertical vs horizontal striations before and after removal of the visual cortex are plotted. The procedure with smaller brightness ratios was slightly modified. In a pilot study it had been found that the operated animals had some difficulties with a brightness ratio of 100 : 13. Therefore the training was now started with the 100 : 1.6 ratio brightness discrimination. Also here the scores with the 100" 1 ratio remained at the 90 o~>
Fig. 5. A typical example of a bilateral lesion of the visual cortex.
261
Fig. 6. A section at the level of the geniculate body of the brain shown in Fig. 5 (Nissl stain).
level in all animals. The average results with the various brightness ratios were determined in the same ways as before the operation. The results are plotted in Fig. 4. The brightness ratio corresponding to the 75 ~o correct level determined by a linear interpolation method [11] was found to be 100:38.7 (S.E. = 2.09). This is significantly different from the 100:59.3 obtained before the operation (Student's t-test P < 0.01). Finally the animals were sacrificed and the brains studied histologically. In Figs. 5 and 6, a typical example of a lesion is shown. In all animals a complete degeneration was seen in the dorsal part of the lateral geniculate nucleus. In spite of the methodological differences between Lashley's study [4] and ours, there is some quantitative agreement between the results. Lashley found that 13 out of 17 normal rats could discriminate a brightness ratio of 2 : 1. Only 2 out of 15 operated rats did as well as this. We found that 11 out of 16 normal rabbits could discriminate a brightness discrimination of 100:50. After the operation only 2 out of 16 were able to do so. As reviewed by LeVere and Morlock [5] several authors have suggested that in the rat a brightness discrimination is normally acquired on the basis of pattern vision mediated by the visual cortex. According to this view the animals relearn the brightness discrimination in a less efficient way on the basis of flux cues [2]. The present results, in which severe impairment of pattern discrimination and an increased threshold of brightness discrimination were found after bilateral removal of the visual cortex, support this view for the rabbit.
262 REFERENCES 1
2 3 4 5 6 7
8 9 10 11
De Vos-Korthals, W.H. and Van Hof, M.W., Pattern discrimination after unilateral and bilateral ablation of the occipital lobe in the rabbit, Behav. Brain Res., 2 (1981) 219-222. Goodale, M. and Cooper, R.M., Cues utilized by normal and posterior neodecorticate rats in the Yerkes brightness discrimination task, Psychon. Sci., 3 (1965) 513-514. Hughes, A. and Vaney, D.I., The organization of binocular cortex in the primary visual are:~ of the rabbit, J, comp. NeuroL, 204 (1982) 151-164. Lashley, K.S., The mechanism of vision: 1I. The influence of cerebral lesions upon the threshold of discrimination for brightness in the rat, J. genet. Psychol., 37 (1930) 461-480. LeVere, T.E. and Morlock, G.W., Nature of visual recovery following posterior neodecortication in the hooded rat, J. comp. physiol. P~vchol., 83 (1973) 62-67. Murphy, E.H. and Chow, K.L., Effects of striate and occipital cortical lesions on visual discrimination in the rabbit, Exp. Neurol., 42 (1974) 78-88. Stuurman, P.M. and Van Hof, M.W., Pattern discrimination in rabbits kept in environments of different complexities after unilateral removal of the occipital cortex, Behav. Brain Res., 1 (1980) 211-226. Van der Mark, F. and Meyer, J.H.C., Automatic control of installations for experiments relating to physiological research of the visual system, Comput. Prog. Biomed., 4 (1974) 35-41. Van Hof, M.W., Discrimination between striated patterns of different orientation in the rabbit, Vision Res., 6 (1966) 89-94. Van Hof, M.W. and Russell, I.S., Binocular vision in the rabbit, Physiol. Behav., 19 (1977) 121-128. Van Hof, M.W. and Wiersma, A.G., The angular threshold of discrimination for striated patterns of different orientation in the rabbit, Vision Res., 7 (1967) 265-270.
257
Elsevier Short Communication Visual discrimination after bilateral removal of the visual cortex in the rabbit
M.W. VAN HOF, J. VAN HOF-VAN DUIN and J.F. HOBBELEN Erasmus Universiteit Rotterdam, Dept. of Physiology I, P.O. Box 1738, Rotterdam (The Netherlands)
(Received February 3rd, 1983) (Revised version received March 15th, 1983) (Accepted April 18th, 1983) Key words: visual discrimination - visual cortex - rabbit
Rabbits were trained on a brightness and a vertical vs horizontal discrimination. After bilateral removal of the visual cortex the threshold of brightness discrimination was significantly higher. In addition, there was a severe impairment of striated pattern discrimination. After bilateral removal of the visual cortex in the rabbit, striated pattern discrimination learning is severely impaired, whilst brightness discrimination learning remains unaffected [6]. Recently, these results were confirmed in a study on two-stage removal of the visual cortex [1]. At the present time a further analysis of the nature of the behavioural deficit after bilateral removal of the visual cortex is in progress in our laboratory. M a n y years ago Lashley [4] described that the threshold of brightness discrimination was considerably lower in normal rats than in rats in which the visual cortex had been removed. The present paper deals with a similar study in the rabbit. Brightness discrimination thresholds were studied quantitatively before and after removal of the visual cortex in the rabbit. From previous experience we knew that in the rabbit bilateral removal of the visual cortex has an unacceptably high postoperative mortality rate. Therefore a two-stage surgical procedure was followed. The pattern discrimination apparatus and the shaping procedure have been described elsewhere [8, 9, 10]. Sixteen Dutch belted rabbits went through the training procedure illustrated in Figs. 1 and 2. The sequence of the training days is plotted on the x-axis, the percentage of correct choices on the y-axis. Throughout training 100 trials were given per day. The procedure started with a brightness discrimination. The brightness ratio between the rewarded and the unrewarded pattern was 100 : 1. The diameter of the targets was 10 cm. After the 90~o correct criterion had been reached on 2 consecutive days training was continued with vertical vs horizontal striations. The diameter of the patterns was 10 cm, the width of the black and white striations, 1.25 cm. After the 90~o 0166-4328/83/$03.00 ~c" 1983 Elsevier Science Publishers B.V.
258
~j~ 10o0
9o
8o
S C)
,
/ ,' /
7o-
,
-,
.-~ i ,oVo
I[
/
6o
.J
< 80
o. DAYS
10
Fig. 1. Example of training procedure in one animal. On the y-axis the percentage of correct choices, on the x-axis the sequence of the days. All animals received 100 trials per day. The procedure started with a brightness discrimination (brightness ratio 100: 1). In all cases the brightest target was rewarded. After the 90,°,0 correct criterion had been reached on 2 consecutive days training was continued with vertical vs horizontal striations. The vertical striations were rewarded. After the 90% criterion had been reached on 2 consecutive days training was continued with various brightness ratios. Fifty trials of the original 100:1 brightness ratio randomly mixed with 50 trials of asmaller brightness ratio were given each day. At first this smaller brightness ratio was 100 : 13. This 100:13 ratio was given for 5 days or less, depending on whether the 90% correct criterion had been reached on 2 consecutive days. Thereafter smaller brightness ratios were used. The second half of the procedure is shown in Fig. 2.
o_ 0
802
oo
o
,3 .01 ~
5o
30
35
40
45
50
~ D A Y S
Fig. 2. The continuation of the training procedure shown in Fig. 1.
criterion had been reached on 2 consecutive days training was resumed on the brightness discrimination but with smaller brightness ratios. Fifty trials of the original 100:1 brightness ratio, randomly mixed with 50 trials of a smaller brightness ratio, were given each day. In all cases the brightest target had a luminance of 0.04 cd per c m 2. The brightest target was always rewarded and placed randomly left or right. As Figs. 1 and 2 show, each of the smaller brightness ratios (100 : 13, 16, 20, 25, 32, 40, 50, 63 and 80) was given for 5 days or less, depending on whether the 90~o correct criterion had been reached on 2 consecutive days. In all animals the percentage of correct choices
259 ©O
100
(0
Do
90 I
~-
80-
~
7O-
~II~
IIl,ll
60 ~
~ 5o 1
2345 ----~
5
to
15
DAYS
Fig. 3. Discrimination with vertical vs horizontal striations before and after bilateral removal of the visual cortex.
with the 100 : 1 brightness ratio remained above the 90% correct level. Since these trials and the ones with the smaller brightness ratios were randomly mixed during the whole procedure it is unlikely that the breakdown of discrimination with the smaller brightness ratios was due to the fact that the animals ignored the patterns. All animals reached the 90~o correct criterion with the initial 100:1 brightness ratio with an average score of 375 (S.E. + 40.3) trials and 91.6 (S.E. + 12.0) errors to criterion. With vertical vs horizontal striations this criterion was reached after 331.3 (S.E. + 32.6) trials, errors to criterion 88.1 (S.E. + 12.1). In Fig, 4, the average percentage of correct choices on the last 2 days of all brightness ratios smaller than 100 : 1 are plotted. In every animal the brightness ratio corresponding with the 75 % correct choices was determined by means of a linear interpolation method [ 11]. The average of these values was 100:59.3 (S.E. + 2.31). After the training procedure was finished a cortical region including the
CO 1 0 0 " LU
0
I L)
90
80"
g 0
70-
:
=NORMAL
~ ' - ~ x A F T E R BILATERAL uJ
60
Z w
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1
1,6
2,5
4
3,2
6,3
5
ABLATION
10
8
16
13
25
20
40
32
63
50
80
Fig. 4. Percentage of correct choices on the y-axis, brightness ratio decreasing from 100' 1 to 100 : 80 on the x-axis.
260 visual cortex [3] and extending beyond V. ! and V.2 [3] was removed unilaterally by means of suction [7]. Three months later the other visual cortex was removed. After a recuperation period of 6 weeks, training was started again. All animals relearned the 100 : 1 brightness discrimination. Criterion was reached with an average score of 287.5 (S.E. _ 43.7) trials and 54.0 (S.E. _ 12.2) errors. Training was continued with vertical vs horizontal striations for 15 days. None of the animals reached the 90 ~o criterion. In Fig. 3, the average scores obtained with vertical vs horizontal striations before and after removal of the visual cortex are plotted. The procedure with smaller brightness ratios was slightly modified. In a pilot study it had been found that the operated animals had some difficulties with a brightness ratio of 100 : 13. Therefore the training was now started with the 100 : 1.6 ratio brightness discrimination. Also here the scores with the 100" 1 ratio remained at the 90 o~>
Fig. 5. A typical example of a bilateral lesion of the visual cortex.
261
Fig. 6. A section at the level of the geniculate body of the brain shown in Fig. 5 (Nissl stain).
level in all animals. The average results with the various brightness ratios were determined in the same ways as before the operation. The results are plotted in Fig. 4. The brightness ratio corresponding to the 75 ~o correct level determined by a linear interpolation method [11] was found to be 100:38.7 (S.E. = 2.09). This is significantly different from the 100:59.3 obtained before the operation (Student's t-test P < 0.01). Finally the animals were sacrificed and the brains studied histologically. In Figs. 5 and 6, a typical example of a lesion is shown. In all animals a complete degeneration was seen in the dorsal part of the lateral geniculate nucleus. In spite of the methodological differences between Lashley's study [4] and ours, there is some quantitative agreement between the results. Lashley found that 13 out of 17 normal rats could discriminate a brightness ratio of 2 : 1. Only 2 out of 15 operated rats did as well as this. We found that 11 out of 16 normal rabbits could discriminate a brightness discrimination of 100:50. After the operation only 2 out of 16 were able to do so. As reviewed by LeVere and Morlock [5] several authors have suggested that in the rat a brightness discrimination is normally acquired on the basis of pattern vision mediated by the visual cortex. According to this view the animals relearn the brightness discrimination in a less efficient way on the basis of flux cues [2]. The present results, in which severe impairment of pattern discrimination and an increased threshold of brightness discrimination were found after bilateral removal of the visual cortex, support this view for the rabbit.
262 REFERENCES 1
2 3 4 5 6 7
8 9 10 11
De Vos-Korthals, W.H. and Van Hof, M.W., Pattern discrimination after unilateral and bilateral ablation of the occipital lobe in the rabbit, Behav. Brain Res., 2 (1981) 219-222. Goodale, M. and Cooper, R.M., Cues utilized by normal and posterior neodecorticate rats in the Yerkes brightness discrimination task, Psychon. Sci., 3 (1965) 513-514. Hughes, A. and Vaney, D.I., The organization of binocular cortex in the primary visual are:~ of the rabbit, J, comp. NeuroL, 204 (1982) 151-164. Lashley, K.S., The mechanism of vision: 1I. The influence of cerebral lesions upon the threshold of discrimination for brightness in the rat, J. genet. Psychol., 37 (1930) 461-480. LeVere, T.E. and Morlock, G.W., Nature of visual recovery following posterior neodecortication in the hooded rat, J. comp. physiol. P~vchol., 83 (1973) 62-67. Murphy, E.H. and Chow, K.L., Effects of striate and occipital cortical lesions on visual discrimination in the rabbit, Exp. Neurol., 42 (1974) 78-88. Stuurman, P.M. and Van Hof, M.W., Pattern discrimination in rabbits kept in environments of different complexities after unilateral removal of the occipital cortex, Behav. Brain Res., 1 (1980) 211-226. Van der Mark, F. and Meyer, J.H.C., Automatic control of installations for experiments relating to physiological research of the visual system, Comput. Prog. Biomed., 4 (1974) 35-41. Van Hof, M.W., Discrimination between striated patterns of different orientation in the rabbit, Vision Res., 6 (1966) 89-94. Van Hof, M.W. and Russell, I.S., Binocular vision in the rabbit, Physiol. Behav., 19 (1977) 121-128. Van Hof, M.W. and Wiersma, A.G., The angular threshold of discrimination for striated patterns of different orientation in the rabbit, Vision Res., 7 (1967) 265-270.