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Visual discrimination after early and late unilateral enucleation of the rabbit
Behavioural Bra#7 Research, 12 (1984) 87-89 Elsevier
87
BBR (10341
Visual discrimination after early and late unilateral enucleation of the rabbit M.W. VAN H O F and P.M. STUURMAN
Department of Physiology 1, Erasmus Universite# Rotterdam, P.O. Box 1738, 3000 DR Rotterdam (The Netherlands) (Received February 17th, 1984) (Revised version received February 29th, 1984) (Accepted March 2nd, 1984)
Key words: early lesions - visual discrimination - enucleation - rabbit
Brightness and tilt discrimination were studied in rabbits in which one eye had been enucleated either 1 day or 3 months after birth. When tested at the age of 5 months no differences in performance were found between both groups of animals.
In the rat, the rabbit, the opossum and the hamster unilateral enucleation shortly after birth affects the structure of the retinofugal pathways ~m.6-~4. Compared with the large number of morphological and electrophysiological studies, relatively little is known & t h e behavioural consequences of early enucleation 5. In the rabbit, Chow et al. 3 have studied the effect of early enucleation. There was no evidence of axonal sprouting in the lateral geniculate body, but uncrossed retinofugal axons spread throughout the lateral half of the superior colliculus in areas normally innervated by the contralateral eye. Electrophysiological studies by the same authors 3 indicated that this abnormal distribution of uncrossed fibres does not make functional synaptic contacts. This abnormal spreading after unilateral enucleation was most pronounced in adult animals enucleated immediately after birth 4. In the present investigation visual discrimination was studied in rabbits in which one eye had been removed either 1 day (n = 21) or 3months (n = 20) after birth. At the age of 5 months, visual discrimination was tested in both groups of animals. The purpose of this study was to find out whether this age-dependent abnormal spreading 0166-4328,/84/$03.00 © 1984 Elsevier Science Publishers B.V.
of the uncrossed retinotectal fibres had any functional consequences. The pattern discrimination apparatus and the shaping procedure have been described elsewhere 15,~6. Throughout training 100 trials were given per day and the food-rewarded pattern was placed randomly either left or right. At first the animals were trained on a brightness discrimination. The white target was rewarded. After the 90 ~o correct criterion was reached, the animals were trained to discriminate vertical vs horizontal striations. The vertical striations were rewarded. After that the minimal angular difference which could be detected by the animals was determined. A total of 2500 trials of vertical vs oblique striations was given. The angular differences used were 45 °, 25 °, 15 °, 10 ° and 5 °. Each angular difference was given for 5 daily sessions of 100 trials. The vertical striations were always rewarded. In random sequence the oblique striations were rotated either clockwise or counter-clockwise. The number of errors to criterion, including the errors made in the series in which the 90 °/o correct level was reached, was determined for brightness and vertical vs horizontal striation discrimination. In addition, the 75 ~o correct value for smaller angles was determined for each animal by means of a
88 TABLE 1 Results after early and late enucleation
1 day operated 3 months operated
Brightness, errors to criterion
Vertical vs horizontal. errors to criterion
75 % correct with smaller angles
128.9 S.E. 18.2 197.7 S.E 34.7
104.6 S.E. 13.5 119.3 S.E. 17.0
16.3 ° S.E. 1.8 16.4 ° S.E. 1.2
linear interpolation m e t h o d 12'~7'2°. In T a b l e I the results for both groups are given. With the Student's-t test, no significant differences were f o u n d for brightness discrimination, vertical vs horizontal discrimination, and 75~o correct levels for smaller angles (p > 0.05). In addition the average score for the last 2 days o f each angular difference w a s o b t a i n e d and c o m bined to provide an average value for b o t h groups. Average values a n d s t a n d a r d errors are plotted in Fig. 1. As the figure shows both curves are in close agreement. tO0•~
90-
~-'~
:
1 DAY 3MONTHS
80-
I-
o
x
70-
U.l r,-
o o
o~
60-
50-
4so
~5o
Cso 1~o ~o
Fig. 1. Average scores and standard errors for the last 2 days of each angular difference. In a previous study on the angular threshold o f tilt discrimination it w a s found that the 7 5 ~ correct level was 9.55 ° S.E. 0.95 ° in n o r m a l rabbits and 14.99 ° S.E. 1.43 ° in rabbits in which a unilateral lesion o f the occipital lobe h a d been m a d C °. This m e a n s that the defect f o u n d after unilateral enucleation in n e w b o r n a n d adult animals is alm o s t identical to that after unilateral ablation of the occipital lobe. During binocular a n d m o n o c u l a r pattern dis-
crimination rabbits h a v e a tendency to expose the t e m p o r a l retina to the patterns ~8A9. Since the u n c r o s s e d fibers arise f r o m this part o f the retina the present results are in agreement with C h o w ' s conclusion that the a b n o r m a l l y spreading u n c r o s s e d fibres do not m a k e functional synaptic contacts.
1 Baisden, R.H. and Shen, C.L, Sprouting of ipsilateral retinal projection in the optic system of the albino rat, Exp. NeuroL, 61 (1978) 549-560. 2 Chalupa, L.M. and Henderson. Z., Monocular enucleation in adult hamsters induces functional changes in the remaining ipsilateral retinotectat projection. Brain Res., 192 (1980) 249-254. 3 Chow, K.L., Mathers, H. and Spear, P.D., Spreading of uncrossed retinal projection in superior colliculus of neonatally enueleated rabbit, J. comp. Neurol., 151 (1973) 307-322. 4 Chow, K.L., Development and reorganization of the uncrossed retinotectal and retinogeniculate fibers in the rabbit. In M.W. van Hof and G. Mohn (Eds.), Functional Recovery from Brain Damage, Elsevier, Amsterdam, t981 pp. 121-129. 5 Ikeda, Y., Yagi, F. and Sakai, M., The role of crossed and uncrossed optic pathways mediating black-white discrimination in rats with one eye enucleated at birth. Physiol. Behav., 30 (1983) 885-890. 6 Fukuda, Y., Sumitomo. I. and Hsiao, C.F.. Effects of neonatal enucteation on excitatory and inhibitory organizations of the albino rat lateral genieulate nucleus, J. Neurophysiol., 50 (1983) 46-60. 7 Lmad, ILD., Uncrossed visual pathways of hooded and albino rats, Science, 149 (1965) 1506-1507. 8 Rhoades, R.W. and Deltacroce. D.D., Neonatal enucleation induces an asymmetric pattern of visual caltosal connections in hamsters, Brain Res., 202 (1980) 189-195. 9 Rhoades. R.W. and Hess, A.. Altered catecholaminergic innervation of superior collJculus after enucleation in adult and neonatal hamsters, Brain Res., 261 (1983) 353-357. 10 Sakai, M. and Yagi, F., Evoked potential in the lateral geniculate body as modified by enucleation of one eye in the albino rat, Brain Res.. 210 (1981l 91-102.
89 11 Sengenlaub, D.R. and Finlay, B.L., Early removal of one eye reduces normally occurring cell death in the remaining eye, Science, 213 (1981) 573-574. 12 Stuurman, P.M., Van Hof, M.W. and Hobbelen, J.F., Behavioural effects of early and late unilateral ablation of the occipital lobe in the rabbit. In M.W. van Hof and G. Mohn (Eds.), Functional Recovery from Brain Damage, Elsevier, Amsterdam, 1981, pp. 121-129. 13 Takeuchi, H., Fukuda, Y. Hara, Y. and Hsiao, C.-F., Physiological properties of expanded ipsilateral retinocollicular projection in neonatally enucleated albino rats, Brain Res., 231 (1982) 191-196. 14 Thompson, I.D., Changes in the uncrossed retinotectal projection after removal of the other eye at birth, Nature (Lond.), 279 (1979) 63-66. 15 Van der Mark, F. and Meyer, J.H.C. Automatic control installations for experiments relating to physiological research of the visual system, Comput. Prog. Biol. Med., 4 (1974) 35-41.
16 Van Hof, M.W., Discrimination between striated patterns of different orientation in the rabbit, Vision Res., 6 (1966) 89-94. 17 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. 18 Van Hof, M.W. and Lagers-van Haselen, G.C., The retinal fixation area in the rabbit, Exp. Neurol., 41 (1973) 218-221. 19 Van Hof, M.W. Interocular transfer and interhemispheric communication in the rabbit. In I. Steele Russell, M.W. van Hof and G. Berlucchi (Eds.), Structure and Function of Cerebral Commissures, MacMillan Press, London, 1979, pp. 224-235. 20 Van Hof, M.W. and Stuurman, P.M., The effect of a unilateral ablation of the occipital lobe on pattern discrimination in the rabbit, Behav. Brain Res., 3 (1981) 401-404.
87
BBR (10341
Visual discrimination after early and late unilateral enucleation of the rabbit M.W. VAN H O F and P.M. STUURMAN
Department of Physiology 1, Erasmus Universite# Rotterdam, P.O. Box 1738, 3000 DR Rotterdam (The Netherlands) (Received February 17th, 1984) (Revised version received February 29th, 1984) (Accepted March 2nd, 1984)
Key words: early lesions - visual discrimination - enucleation - rabbit
Brightness and tilt discrimination were studied in rabbits in which one eye had been enucleated either 1 day or 3 months after birth. When tested at the age of 5 months no differences in performance were found between both groups of animals.
In the rat, the rabbit, the opossum and the hamster unilateral enucleation shortly after birth affects the structure of the retinofugal pathways ~m.6-~4. Compared with the large number of morphological and electrophysiological studies, relatively little is known & t h e behavioural consequences of early enucleation 5. In the rabbit, Chow et al. 3 have studied the effect of early enucleation. There was no evidence of axonal sprouting in the lateral geniculate body, but uncrossed retinofugal axons spread throughout the lateral half of the superior colliculus in areas normally innervated by the contralateral eye. Electrophysiological studies by the same authors 3 indicated that this abnormal distribution of uncrossed fibres does not make functional synaptic contacts. This abnormal spreading after unilateral enucleation was most pronounced in adult animals enucleated immediately after birth 4. In the present investigation visual discrimination was studied in rabbits in which one eye had been removed either 1 day (n = 21) or 3months (n = 20) after birth. At the age of 5 months, visual discrimination was tested in both groups of animals. The purpose of this study was to find out whether this age-dependent abnormal spreading 0166-4328,/84/$03.00 © 1984 Elsevier Science Publishers B.V.
of the uncrossed retinotectal fibres had any functional consequences. The pattern discrimination apparatus and the shaping procedure have been described elsewhere 15,~6. Throughout training 100 trials were given per day and the food-rewarded pattern was placed randomly either left or right. At first the animals were trained on a brightness discrimination. The white target was rewarded. After the 90 ~o correct criterion was reached, the animals were trained to discriminate vertical vs horizontal striations. The vertical striations were rewarded. After that the minimal angular difference which could be detected by the animals was determined. A total of 2500 trials of vertical vs oblique striations was given. The angular differences used were 45 °, 25 °, 15 °, 10 ° and 5 °. Each angular difference was given for 5 daily sessions of 100 trials. The vertical striations were always rewarded. In random sequence the oblique striations were rotated either clockwise or counter-clockwise. The number of errors to criterion, including the errors made in the series in which the 90 °/o correct level was reached, was determined for brightness and vertical vs horizontal striation discrimination. In addition, the 75 ~o correct value for smaller angles was determined for each animal by means of a
88 TABLE 1 Results after early and late enucleation
1 day operated 3 months operated
Brightness, errors to criterion
Vertical vs horizontal. errors to criterion
75 % correct with smaller angles
128.9 S.E. 18.2 197.7 S.E 34.7
104.6 S.E. 13.5 119.3 S.E. 17.0
16.3 ° S.E. 1.8 16.4 ° S.E. 1.2
linear interpolation m e t h o d 12'~7'2°. In T a b l e I the results for both groups are given. With the Student's-t test, no significant differences were f o u n d for brightness discrimination, vertical vs horizontal discrimination, and 75~o correct levels for smaller angles (p > 0.05). In addition the average score for the last 2 days o f each angular difference w a s o b t a i n e d and c o m bined to provide an average value for b o t h groups. Average values a n d s t a n d a r d errors are plotted in Fig. 1. As the figure shows both curves are in close agreement. tO0•~
90-
~-'~
:
1 DAY 3MONTHS
80-
I-
o
x
70-
U.l r,-
o o
o~
60-
50-
4so
~5o
Cso 1~o ~o
Fig. 1. Average scores and standard errors for the last 2 days of each angular difference. In a previous study on the angular threshold o f tilt discrimination it w a s found that the 7 5 ~ correct level was 9.55 ° S.E. 0.95 ° in n o r m a l rabbits and 14.99 ° S.E. 1.43 ° in rabbits in which a unilateral lesion o f the occipital lobe h a d been m a d C °. This m e a n s that the defect f o u n d after unilateral enucleation in n e w b o r n a n d adult animals is alm o s t identical to that after unilateral ablation of the occipital lobe. During binocular a n d m o n o c u l a r pattern dis-
crimination rabbits h a v e a tendency to expose the t e m p o r a l retina to the patterns ~8A9. Since the u n c r o s s e d fibers arise f r o m this part o f the retina the present results are in agreement with C h o w ' s conclusion that the a b n o r m a l l y spreading u n c r o s s e d fibres do not m a k e functional synaptic contacts.
1 Baisden, R.H. and Shen, C.L, Sprouting of ipsilateral retinal projection in the optic system of the albino rat, Exp. NeuroL, 61 (1978) 549-560. 2 Chalupa, L.M. and Henderson. Z., Monocular enucleation in adult hamsters induces functional changes in the remaining ipsilateral retinotectat projection. Brain Res., 192 (1980) 249-254. 3 Chow, K.L., Mathers, H. and Spear, P.D., Spreading of uncrossed retinal projection in superior colliculus of neonatally enueleated rabbit, J. comp. Neurol., 151 (1973) 307-322. 4 Chow, K.L., Development and reorganization of the uncrossed retinotectal and retinogeniculate fibers in the rabbit. In M.W. van Hof and G. Mohn (Eds.), Functional Recovery from Brain Damage, Elsevier, Amsterdam, t981 pp. 121-129. 5 Ikeda, Y., Yagi, F. and Sakai, M., The role of crossed and uncrossed optic pathways mediating black-white discrimination in rats with one eye enucleated at birth. Physiol. Behav., 30 (1983) 885-890. 6 Fukuda, Y., Sumitomo. I. and Hsiao, C.F.. Effects of neonatal enucteation on excitatory and inhibitory organizations of the albino rat lateral genieulate nucleus, J. Neurophysiol., 50 (1983) 46-60. 7 Lmad, ILD., Uncrossed visual pathways of hooded and albino rats, Science, 149 (1965) 1506-1507. 8 Rhoades, R.W. and Deltacroce. D.D., Neonatal enucleation induces an asymmetric pattern of visual caltosal connections in hamsters, Brain Res., 202 (1980) 189-195. 9 Rhoades. R.W. and Hess, A.. Altered catecholaminergic innervation of superior collJculus after enucleation in adult and neonatal hamsters, Brain Res., 261 (1983) 353-357. 10 Sakai, M. and Yagi, F., Evoked potential in the lateral geniculate body as modified by enucleation of one eye in the albino rat, Brain Res.. 210 (1981l 91-102.
89 11 Sengenlaub, D.R. and Finlay, B.L., Early removal of one eye reduces normally occurring cell death in the remaining eye, Science, 213 (1981) 573-574. 12 Stuurman, P.M., Van Hof, M.W. and Hobbelen, J.F., Behavioural effects of early and late unilateral ablation of the occipital lobe in the rabbit. In M.W. van Hof and G. Mohn (Eds.), Functional Recovery from Brain Damage, Elsevier, Amsterdam, 1981, pp. 121-129. 13 Takeuchi, H., Fukuda, Y. Hara, Y. and Hsiao, C.-F., Physiological properties of expanded ipsilateral retinocollicular projection in neonatally enucleated albino rats, Brain Res., 231 (1982) 191-196. 14 Thompson, I.D., Changes in the uncrossed retinotectal projection after removal of the other eye at birth, Nature (Lond.), 279 (1979) 63-66. 15 Van der Mark, F. and Meyer, J.H.C. Automatic control installations for experiments relating to physiological research of the visual system, Comput. Prog. Biol. Med., 4 (1974) 35-41.
16 Van Hof, M.W., Discrimination between striated patterns of different orientation in the rabbit, Vision Res., 6 (1966) 89-94. 17 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. 18 Van Hof, M.W. and Lagers-van Haselen, G.C., The retinal fixation area in the rabbit, Exp. Neurol., 41 (1973) 218-221. 19 Van Hof, M.W. Interocular transfer and interhemispheric communication in the rabbit. In I. Steele Russell, M.W. van Hof and G. Berlucchi (Eds.), Structure and Function of Cerebral Commissures, MacMillan Press, London, 1979, pp. 224-235. 20 Van Hof, M.W. and Stuurman, P.M., The effect of a unilateral ablation of the occipital lobe on pattern discrimination in the rabbit, Behav. Brain Res., 3 (1981) 401-404.