Physiology & Behavior, Vol. 19, pp. 425-428. Pergamon Press and Brain Research Publ., 1977. Printed in the U.S.A.
Failure of Interocular Transfer in the Pigeon
(Columba livia) J. A. GRAVES AND M. A. GOODALE
Psychological Laborato~, Universi~ o f St. Andrews, St. Andrews, Fife, Scotland (Received 28 February 1977) GRAVES, J. A. AND M. A. GOODALE. Failure ofinterocular transfer in the pigeon (Columba livia). PHYSIOL. BEHAV. 19(3) 425-428, 1977. - Pigeons were trained on a modified jumping stand to discriminate a circle from a triangle using only one eye. Testing with the naive eye revealed no evidence of interocular transfer. This failure of transfer was also observed under more stringent testing using reversal learning. The results are discussed in terms of a selective attention model for panoramic vision. Interocular transfer
Pigeon
Visual discrimination
Visual system
Reversal learning
without exception, subsequent investigations of interocular transfer in the pigeon have involved the use of illuminated keys and the pecking response. There has been no attempt to replicate the original jumping stand experiments. Therefore, the present experiment was designed to examine the Levine findings in the same jumping stand situation but using a more sensitive reversal transfer procedure. In addition, a training and testing programme was used which helped to ensure that the pigeons were attending to the locus of the discriminative stimuli and were also capable of making the appropriate jumping response.
OVER thirty years ago, Levine [ 1 4 - 1 6 ] reported that pigeons which had been trained monocularly on a visual discrimination task would show evidence of learning with the naive eye only .when the stimuli had been presented "to certain parts of the visual .field. Using a modification of the Lashley jumping stand, he showed that there was no interocular transfer of brightness, colour, or pattern discriminations when the stimuli were presented vertically in front of the pigeon (aflterostral position) but that there was transfer when the discriminanda were presented below the pigeon's head (subrostral position). Moreover, he found that discrimination broke down when the stimulus cards were shifted to the anterostral position after the birds had been trained with both eyes open to respond to these same cards in the subrostral position. In striking contrast to these findings, Catania [6], using an operant conditioning method, found complete interocular transfer of brightness, colour, and pattern discriminations regardless of whether the stimuli had been located forward or laterally in t h e pigeon's visual field. This observation has since been confirmed repeatedly [9, 17, 19]. Catania suggested that one possible explanation for the difference between his and Levine's results could be derived from the characteristics of the pigeon's visual system. He argued [5] that the pigeon is laterally far-sighted and anteriorly near-sighted. Therefore, in order to view the anterostral stimuli, Levine's pigeons had to cock their heads to one side and bring the stimuli into the lateral field. Since the head would be cocked to the left or right depending on which eye was covered, the jumping response in each case might also have been different. Thus, when the eye-cover was switched from one eye to the other for the first time, the necessary change in posture could have affected the interocular transfer results since the pigeon would not be able to jump in the same way as it had before. Nevertheless, it could still he argued that Levine's results do represent a true failure of interocular transfer. Almost
METHOD .
Animals Six naive homing pigeons (Columba livia) weighing approximately 425 g were used. The birds were housed individually and were maintained on ad lib food and water throughout the experiment.
Apparatus An attempt was made to reproduce the jumping stand used by Levine [I 1,14]. A rotating perch 45 cm in length was constructed from a 2.5 cm diameter rod and was covered with rough cloth. Two collapsible platforms measuring 19 x 14 cm were located 7 cm in front of and 5 cm below the perch. The platforms could be independently locked in position by clips located on the outside of the apparatus so that either one could be made secure or allowed to collapse when a bird landed on it. A 10 cm partition separated the two platforms allowing a pigeon to jump to one or the other but not to both platforms at once. Stimulus cards measuring 19 x 14 cm were positioned on the surface of the platforms themselves as well as vertically on the wall of the apparatus directly behind the platforms. The cards, which could be moved from one 425
426 platform and wall to the other, contained either a white outline triangle or circle on a flat black background. The figures were equated for luminous flux. The platforms and perch were enclosed in a box 45 cm wide, 34 cm deep and 90 cm high. The perch was located 25 cm above the floor of the box and could be rotated by means of a large wheel attached to the outside of the box. The entire apparatus except for the stimulus cards was painted matt grey. Illumination was provided by two 100W light bulbs suspended approximately 1 m above the open top of the apparatus. In addition, the testing room housing the apparatus was itself illuminated by fluorescent lighting. The blindfold for monocular training was made from black cloth which fitted over the beak of the bird and fastened behind the bird's head. The area around one eye was left open and was surrounded by a thin metal ring attached to the cloth blindfold. A foam pad was located over the closed eye under the blindfold. As far as could be determined, such an arrangement neither obstructed vision on the open side nor allowed any light through the closed side. Blindfolds covering the left or the right eye were used throughout the entire experiment. A blindfold was put on 5 rain before a daily training session and was removed immediately afterwards.
Train ing Each pigeon was given 20 trials a day on the jumping stand. On each trial, a pigeon was placed on the perch which was then rotated forcing it to jump to one of the two platforms. If the pigeon jumped onto the correct platform, it was allowed to stay there for 15 sec. If it jumped onto the incorrect one, the platform would collapse and the pigeon would fall 20 cm into a pile of hay placed in the bottom of the apparatus. The pigeon was then picked up immediately. A noncorrection procedure was employed with an intertrial interval of approximately 30 sec in which the bird was held in the experimenter's hand outside the apparatus. The stimulus cards were switched from right to left in accordance with a pseudorandom sequence. Training was continued on each discrimination task until the criterion of 18 trials correct in one day was reached.
Design The training of each bird took place in 4 stages. Both eyes were trained successively to criterion on the triangle vs circle discrimination, and then both eyes were trained successively to criterion on the reversal of that discrimination. This procedure is summarised for one of the pigeons in Fig. 1. As the figure shows, during Stage 1 this bird was trained with the right eye covered and triangle positive until it reached criterion. During Stage 2, the left eye was covered and the bird was trained with triangle positive again. After reaching criterion, the bird was shifted to Stage 3 in which the left eye was still occluded, but now the circle was the positive stimulus. In Stage 4, the blindfold was switched back to the right eye, and the bird was trained with the circle positive once more. For one half of the birds, the triangle was positive during Stages 1 and 2, and for one half, the circle was positive. In addition, one half of the birds began learning the discrimination with the left eye covered and one half with the right eye covered. Immediately before both Stages 1 and 2 each bird was given 20 pretraining trials a day for 2 days in which both
GRAVES AND GOODALE
STAGES 1
2
6, AO
AO
÷
÷
3
4
6,
AO +
AO +
FIG. 1. Four stages of training. The solid crescent indicates the position of the blindfold. The plus sign marks the positive stimulus in each stage. platforms were secured and the stimulus cards were plain black. In each of these pretraining sessions, the bird was trained to j u m p using only that eye which was to be unoccluded in the subsequent training stage. A retention test was inserted between Stages 3 and 4. This test consisted of 2 daily sessions of 20 trials during which neither platform would collapse. However, the triangle and circle were still shifted from left to right according to the pseudo-random sequence. The trials were given in blocks of 5 with the blindfold switched after each block of 5 trials. This meant that during each daily session, the pigeon had 10 trials with the right eye occluded a n d 10 trials with the left eye occluded. Each time the blindfold was switched, the pigeon was allowed to sit outside the apparatus for 10 min. RESULTS As Table 1 illustrates, the pigeons did not make significantly fewer errors in Stage 2 than they did in Stage 1 of the experiment. Furthermore, there was no significant difference between the number of days required by the birds to reach criterion on the task in Stages 1 and 2. They took as long to learn the task with the second eye as they did with the first. A similar relationship exists between Stages 3 and 4. There was no significant difference in either errors or days to criterion. However, analysis of variance revealed that the birds made significantly more errors (q = 3.70, p< 0.05) and took significantly longer (p< 0.05) to learn the reversal task in Stage 4, t h a n they did to learn the original discrimination in Stage I. On the retention test inserted between Stages 3 and 4. the birds chose the stimulus that had been correct m Stage 3 when they were allowed to use that eye that had been uncovered in Stage 3. However. when they were forced to use the other eye they chose the stimulus that had been correct in Stages 1 and 2. Although the pattern of responding was more consistent when the birds were using the eye that had been trained most recently, the choice of stimuli using either eye was significantly different from chance (sign test: p = 0.016 and p = 0.031). DISCUSSION The results of the present experiment provide a strong
FAILURE OF INTEROCULAR TRANSFER
427
Idd ft.
7
8
9
10
11
12
PIGEONS FIG. 2. The performance of each pigeon on the retention test inserted between Stages 3 and 4. The height of each bar indicates the percentage of trials on which the stimulus that had most recently been correct for that eye was chosen. The performance of each pigeon using the eye that had been last trained in Stage 1 is represented by a solid bar and the performance with the eye last trained in Stage 3 is represented by an open bar.
TABLE 1 STAGE 1
STAGS 2 |lUtOItS DAYS
STAGE 3 tltlltOtS
DAYS
STAGE 4
PrOtON
|ltl~tS
DAYS
EtltOItS DAYS
7
292
36
194
24
29s
33
283
37
8
197
25
196
22
2s7
32
187
25
9
259
33
2s6
33
aso
43
368
39
10
lqDo
22
196
24
22~
25
286
3~t
11
173
21
87
is
310
33
341
38
12
189
22
202
24
2~Jo
29
267
28
216.7
26.S
181LS 2 ~ 7
~
a2~s
28a.7
~J.2
confirmation of Levine's [ 14] earlier reports of failure of interocular transfer in pigeons trained on a j u m p i n g stand. Furthermore, the failure of transfer between Stages 3 and 4 is inconsistent with Catania's [5,6] proposal that the subsequent change in posture following switching of eyecovers is responsible for the poor performance of the discrimination habit. During Stage 4, the pigeons were using the eye that they had already used on a large n u m b e r of trials during Stage 1 and were well accustomed to the apparatus. Nevertheless, contrary to what Catania might have predicted, these birds failed to learn the discrimination reversal in Stage 4 any faster than they had in Stage 3 using the other eye. I n d e e d , the performances in both these stages were highly similar and during the early portion of both stages, the pigeons jumped towards the previously positive stimulus a considerable n u m b e r of times before they began to jump to the correct platform. The results of the retention test administered between Stages 3 and 4 also indicate that in the jumping stand
situation there is no evidence for interocular transfer in the pigeon. When tested with the eye that had been uncovered during Stage l, the pigeons jumped towards the stimulus that had been negative during Stage 3, even though they had not been trained with that eye for an average of I 120 trials. In fact, in the last 660 of those trials, they had been trained with the other eye not to jump towards that stimulus, but towards the other one. It could be argued that the pigeons had simply learned a conditional discrimination, jumping to either stimulus depending on which eye was uncovered. Certainly both Catania [6] and Konnerman [13] have demonstrated that it is possible to train birds on conflicting discriminations using each eye separately in situations where there is normally good interocular transfer. However, Catania alternated the training sessions for each eye from day to day, whereas in the present experiment the pigeons were trained to criterion on one eye before being switched to the other. Konnerman failed to establish conflicting discriminations in domestic geese when one eye was trained to criterion first, even though he was able to do so when the geese were given alternate sessions for the left and fight eyes in the same day. This suggests that the pigeons' behaviour in the interpolated retention test of the present experiment was not the result of having learned a conditional and conflicting discrimination, but was a reflection of the absence of interocular transfer in the situation. Catania [6] suggested that one reason why he found transfer and Levine did not could be the difference in the number of responses required f o r learning in their respective training situations. Since Catania required his pigeons to make many thousands of responses, the resultant overtraining may have been responsible for the successful transfer from one eye to the other. However, the n u m b e r of trials to criterion required in "each stage of the present experiment was quite comparable to the number of responses made by pigeons in Meier's experiments [17] where he found transfer on both colour and pattern discriminations using a two-choice operant procedure. In our own laboratory, pigeons monocularly trained on a colour discrimination in a two-choice operant procedure show good interocular transfer in a training and testing paradigm identical to that used on the j u m p i n g stand even though the total n u m b e r of responses made in the key-pecking task was much less (Graves and Goodale, unpublished observations). The reasons for the absence or presence of interocular transfer in different situations are not at all clear. A n u m b e r of investigators have observed failure of transfer in birds trained on tasks other than jumping stands. Using an appetitive task in which pigeons had to approach the stimuli from some distance, Beritov and Chichinadze [3,7] found no evidence for interocular transfer of either colour or pattern discriminations. Zeie]: [26] found that chicks which had been monocularly habituated to the deep side of a visual cliff, showed depth avoidance when tested with the naive eye, but not with the trained eye. Similarly, Benowitz [1,2] has reported that although a monocularly learned suppression of pecking at distasteful objects did show good transfer in chickens, the extinction of the suppression did not. Ingle [ 12] has observed in the goldfish that a simple line orientation discrimination showed interocular transfer whereas a more difficult one did not. Indeed, in both fish and birds, the information transferred to the untrained eye frequently seems to be less complete than. that available to
428
GRAVES AND GOODALE
the trained eye. Thus both chickens and carp failed to show transfer of shape discriminations when the stimuli were altered from the original, even though they could discriminate the altered shapes with the trained eye [ 18,22]. Under certain training conditions, mammals with visual projections that are highly crossed such as the rabbit and the rat have shown very poor interocular transfer [8, 23-25]. It is evident from these and other experiments that there are probably a number of different factors affecting interocular transfer including exposure time, task difficulty, and the presence of irrelevant stimuli in the visual field of the untrained eye [ 12,20]. But it is difficult to see how any of these factors would easily explain the difference in interocular transfer found between pigeons trained on a jumping stand and those in a Skinner box. However, one probable difference between the two situations lies in the parts of the visual system used by the pigeon in each case; a distinction anticipated much earlier by Levine [151 and restated by Catania [ 4 - 6 1 in a different explanatory context. In the jumping stand, the pigeons were some distance from the dtscriminanda, approximately 15 cm (from the upright stimulus but less for the horizontal) and may therefore have used the lateral visual field to inspect the stimulus array since they are laterally far sighted. In the Skinner box, however, since the
birds were much closer to the stimulus keys and were also directing pecks at these keys, they were perhaps more likely to use that part of the visual field which in normal circumstances is binocularly represented. The lateral visual fields in an animal with panoramic vision, such as the pigeon, would represent two very different views of the world. Therefore, it might be expected that if only one of these fields included stimuli which were controlling behaviour, then some sort of selective attention by either unilateral suppression and/or emphasis of input could be operating. Certainly there is electrophysiological evidence for the existence of a commissural inhibitory mechanism in the optic tectum of the pigeon [21 ] and several mammalian species [10]. The failure of transfer in the jumping stand could therefore be a reflection of the operation of such inhibitory circuits. In contrast, the processing of visual information falling on those parts of the visual field which are binocularly represented would not be expected to require the participation of selective attention mechanisms. Consequently discriminative stimuli which are presented to this part of the visual field of one eye might show good interocular transfer to the other. However, this line of reasoning remains highly speculative until there is direct cine film or videotape analysis of the scanning and visual search patterns of pigeons in each of these situations.
REFERENCES
I. Benowitz, L. Effects of forebrain ablations on avoidance learning in chicks. PhysioL Behav. 9: 601-608, 1972. 2. Benowitz, L. Conditions for the bilateral transfer of monocular learning in chicks. Brain Res. 65: 203-213, 1974. 3. Beritov, J. S. and N. Chichinadze. Localization of visual perception in the pigeon. Bull. exp. BioL Med. U.S.S.R. 2: 105-107, 1936. 4. Catania, A. C. Techniques for control of monocular and binocular viewing in the pigeon. J. exp. Anal Behav. 6: 627-629, 1963. 5. Catania, A. C. On the visual acuity of the pigeon. J. exp. Anal Behav. 7: 361-366, 1964. 6. Catania, A. C. Interocular transfer of discriminations in the pigeon. J. exp. Anal Behav. 8: 147-155, 1965. 7. Chichinadze, N. Das Problem der Lokalisation kortikaler Prozesse, welche durch optisehe Reize hervorgerufen werden. Mitt. Georgischen Abt. Akad. Viss. U.S.S.R. 1: 609-614, 1940. 8. Cowey, A. and A. M. Parkinson. Effects of sectioning the corpus callosum on interocular transfer in hooded rats. Expl Brain Res. 18: 433-445, 1973. 9. Cuenod, M. and H. Zeier. Transfer interhemispherique et commissurotomie chez le pigeon. Schweiz. Arch. NeuroL Neurochir. Psychiat. 100: 365-380, 1967. 10. Goodale, M. A. Cortico-tectal and intertectal modulation of visual responses in the rat's superior coUiculus. Expl Brain Res. 17: 75-86, 1973. 11. Halstead, W. and G. Yacorzynski. A jumping method for establishing differential responses in pigeons. £ Genet. PsychoL 52: 227-231, 1938. 12. Ingle, D. lnterocular integration of visual learning by goldfish. Brain Behav. Evol. 1: 58-85, 1968. 13. Konnerman, G. Monokulare Dressur yon Hausgffnsen, z. T. mit entgegengesetzter Merkmalsbedeutung ftir beide Augen. Z 77erp~choL 23: 555-580. 1966.
14. Levine, J. Studies in interrelations of central nervous structures in binocular vision. Lack of bilateral transfer of visual discrimination habits acquired monocularly by the pigeon. J. Genet. PsychoL 67: 105-129, 1945. 15. Levine, J., II. Conditions under which interocular transfer of discrimination habits takes place in the pigeon, d. Genet. Psyehol. 67: 131-142, 1945. 16. Levine, J. III.Localization of memory trace as evidenced by lack of inter- and intra-ocular habit transfer in the pigeon. J. Genet. Psychol. 81: 19-27, 1952. 17. Meier, R. E. Interhemisph~riscber Transfer visueiler Zweifachwahlen bei kommissurotomierten Tauben. Psychol. Forsch. 34: 220-245, 1971. 18. Menkhaus, 1. Verscuhe tiber einiiugiges Lernen und Transponieren beim Haushuhn. Z. Tierpsychol. 14: 210-230, 195.7. 19. Ogawa, T. and S. Ohinata. Interocular transfer of colour discrimination in the pigeon. Ann. Anim. PsychoL Tokyo 16: 1-9, 1966. 20. Palmers, C. and H. Zeier. Hemispheric dominance and transfer in the pigeon. Brain Res. 76: 537"541, 1974. 21. Robert, F. and M. Cuenod. Electrophysiology of intertectal commissures in the pigeon II. inhibitory interaction. Expl Brain Res. 9: 116-136, 1969. 22. Schulte, A. Transfer und transpositionsversuche mit monokulardressierten Fiscben. Z. vergl. Physiol. 39: 432-476, 1957. 23. Steele-Rus~ll, I. and J. F. Safferstone. Interocular transfer and stimulus control of visual discriminations in the rat. Brain Res. 66: 355-356, 1974. 24. Van Hof, M. W. Interocular transfer in the rabbit. Expl Neurol. 26: 103-108, 1970. 25. Van Hof, M. W. and F. van der Mark. A quantitative study on interocular transfer in the rabbit. Physiol. Behav. 16: 775-782, 1976. 26. Zeier, H. Lack of eye-to-eye transfer of an early response modification. Nature 225: 708-709, 1970.
Failure of Interocular Transfer in the Pigeon
(Columba livia) J. A. GRAVES AND M. A. GOODALE
Psychological Laborato~, Universi~ o f St. Andrews, St. Andrews, Fife, Scotland (Received 28 February 1977) GRAVES, J. A. AND M. A. GOODALE. Failure ofinterocular transfer in the pigeon (Columba livia). PHYSIOL. BEHAV. 19(3) 425-428, 1977. - Pigeons were trained on a modified jumping stand to discriminate a circle from a triangle using only one eye. Testing with the naive eye revealed no evidence of interocular transfer. This failure of transfer was also observed under more stringent testing using reversal learning. The results are discussed in terms of a selective attention model for panoramic vision. Interocular transfer
Pigeon
Visual discrimination
Visual system
Reversal learning
without exception, subsequent investigations of interocular transfer in the pigeon have involved the use of illuminated keys and the pecking response. There has been no attempt to replicate the original jumping stand experiments. Therefore, the present experiment was designed to examine the Levine findings in the same jumping stand situation but using a more sensitive reversal transfer procedure. In addition, a training and testing programme was used which helped to ensure that the pigeons were attending to the locus of the discriminative stimuli and were also capable of making the appropriate jumping response.
OVER thirty years ago, Levine [ 1 4 - 1 6 ] reported that pigeons which had been trained monocularly on a visual discrimination task would show evidence of learning with the naive eye only .when the stimuli had been presented "to certain parts of the visual .field. Using a modification of the Lashley jumping stand, he showed that there was no interocular transfer of brightness, colour, or pattern discriminations when the stimuli were presented vertically in front of the pigeon (aflterostral position) but that there was transfer when the discriminanda were presented below the pigeon's head (subrostral position). Moreover, he found that discrimination broke down when the stimulus cards were shifted to the anterostral position after the birds had been trained with both eyes open to respond to these same cards in the subrostral position. In striking contrast to these findings, Catania [6], using an operant conditioning method, found complete interocular transfer of brightness, colour, and pattern discriminations regardless of whether the stimuli had been located forward or laterally in t h e pigeon's visual field. This observation has since been confirmed repeatedly [9, 17, 19]. Catania suggested that one possible explanation for the difference between his and Levine's results could be derived from the characteristics of the pigeon's visual system. He argued [5] that the pigeon is laterally far-sighted and anteriorly near-sighted. Therefore, in order to view the anterostral stimuli, Levine's pigeons had to cock their heads to one side and bring the stimuli into the lateral field. Since the head would be cocked to the left or right depending on which eye was covered, the jumping response in each case might also have been different. Thus, when the eye-cover was switched from one eye to the other for the first time, the necessary change in posture could have affected the interocular transfer results since the pigeon would not be able to jump in the same way as it had before. Nevertheless, it could still he argued that Levine's results do represent a true failure of interocular transfer. Almost
METHOD .
Animals Six naive homing pigeons (Columba livia) weighing approximately 425 g were used. The birds were housed individually and were maintained on ad lib food and water throughout the experiment.
Apparatus An attempt was made to reproduce the jumping stand used by Levine [I 1,14]. A rotating perch 45 cm in length was constructed from a 2.5 cm diameter rod and was covered with rough cloth. Two collapsible platforms measuring 19 x 14 cm were located 7 cm in front of and 5 cm below the perch. The platforms could be independently locked in position by clips located on the outside of the apparatus so that either one could be made secure or allowed to collapse when a bird landed on it. A 10 cm partition separated the two platforms allowing a pigeon to jump to one or the other but not to both platforms at once. Stimulus cards measuring 19 x 14 cm were positioned on the surface of the platforms themselves as well as vertically on the wall of the apparatus directly behind the platforms. The cards, which could be moved from one 425
426 platform and wall to the other, contained either a white outline triangle or circle on a flat black background. The figures were equated for luminous flux. The platforms and perch were enclosed in a box 45 cm wide, 34 cm deep and 90 cm high. The perch was located 25 cm above the floor of the box and could be rotated by means of a large wheel attached to the outside of the box. The entire apparatus except for the stimulus cards was painted matt grey. Illumination was provided by two 100W light bulbs suspended approximately 1 m above the open top of the apparatus. In addition, the testing room housing the apparatus was itself illuminated by fluorescent lighting. The blindfold for monocular training was made from black cloth which fitted over the beak of the bird and fastened behind the bird's head. The area around one eye was left open and was surrounded by a thin metal ring attached to the cloth blindfold. A foam pad was located over the closed eye under the blindfold. As far as could be determined, such an arrangement neither obstructed vision on the open side nor allowed any light through the closed side. Blindfolds covering the left or the right eye were used throughout the entire experiment. A blindfold was put on 5 rain before a daily training session and was removed immediately afterwards.
Train ing Each pigeon was given 20 trials a day on the jumping stand. On each trial, a pigeon was placed on the perch which was then rotated forcing it to jump to one of the two platforms. If the pigeon jumped onto the correct platform, it was allowed to stay there for 15 sec. If it jumped onto the incorrect one, the platform would collapse and the pigeon would fall 20 cm into a pile of hay placed in the bottom of the apparatus. The pigeon was then picked up immediately. A noncorrection procedure was employed with an intertrial interval of approximately 30 sec in which the bird was held in the experimenter's hand outside the apparatus. The stimulus cards were switched from right to left in accordance with a pseudorandom sequence. Training was continued on each discrimination task until the criterion of 18 trials correct in one day was reached.
Design The training of each bird took place in 4 stages. Both eyes were trained successively to criterion on the triangle vs circle discrimination, and then both eyes were trained successively to criterion on the reversal of that discrimination. This procedure is summarised for one of the pigeons in Fig. 1. As the figure shows, during Stage 1 this bird was trained with the right eye covered and triangle positive until it reached criterion. During Stage 2, the left eye was covered and the bird was trained with triangle positive again. After reaching criterion, the bird was shifted to Stage 3 in which the left eye was still occluded, but now the circle was the positive stimulus. In Stage 4, the blindfold was switched back to the right eye, and the bird was trained with the circle positive once more. For one half of the birds, the triangle was positive during Stages 1 and 2, and for one half, the circle was positive. In addition, one half of the birds began learning the discrimination with the left eye covered and one half with the right eye covered. Immediately before both Stages 1 and 2 each bird was given 20 pretraining trials a day for 2 days in which both
GRAVES AND GOODALE
STAGES 1
2
6, AO
AO
÷
÷
3
4
6,
AO +
AO +
FIG. 1. Four stages of training. The solid crescent indicates the position of the blindfold. The plus sign marks the positive stimulus in each stage. platforms were secured and the stimulus cards were plain black. In each of these pretraining sessions, the bird was trained to j u m p using only that eye which was to be unoccluded in the subsequent training stage. A retention test was inserted between Stages 3 and 4. This test consisted of 2 daily sessions of 20 trials during which neither platform would collapse. However, the triangle and circle were still shifted from left to right according to the pseudo-random sequence. The trials were given in blocks of 5 with the blindfold switched after each block of 5 trials. This meant that during each daily session, the pigeon had 10 trials with the right eye occluded a n d 10 trials with the left eye occluded. Each time the blindfold was switched, the pigeon was allowed to sit outside the apparatus for 10 min. RESULTS As Table 1 illustrates, the pigeons did not make significantly fewer errors in Stage 2 than they did in Stage 1 of the experiment. Furthermore, there was no significant difference between the number of days required by the birds to reach criterion on the task in Stages 1 and 2. They took as long to learn the task with the second eye as they did with the first. A similar relationship exists between Stages 3 and 4. There was no significant difference in either errors or days to criterion. However, analysis of variance revealed that the birds made significantly more errors (q = 3.70, p< 0.05) and took significantly longer (p< 0.05) to learn the reversal task in Stage 4, t h a n they did to learn the original discrimination in Stage I. On the retention test inserted between Stages 3 and 4. the birds chose the stimulus that had been correct m Stage 3 when they were allowed to use that eye that had been uncovered in Stage 3. However. when they were forced to use the other eye they chose the stimulus that had been correct in Stages 1 and 2. Although the pattern of responding was more consistent when the birds were using the eye that had been trained most recently, the choice of stimuli using either eye was significantly different from chance (sign test: p = 0.016 and p = 0.031). DISCUSSION The results of the present experiment provide a strong
FAILURE OF INTEROCULAR TRANSFER
427
Idd ft.
7
8
9
10
11
12
PIGEONS FIG. 2. The performance of each pigeon on the retention test inserted between Stages 3 and 4. The height of each bar indicates the percentage of trials on which the stimulus that had most recently been correct for that eye was chosen. The performance of each pigeon using the eye that had been last trained in Stage 1 is represented by a solid bar and the performance with the eye last trained in Stage 3 is represented by an open bar.
TABLE 1 STAGE 1
STAGS 2 |lUtOItS DAYS
STAGE 3 tltlltOtS
DAYS
STAGE 4
PrOtON
|ltl~tS
DAYS
EtltOItS DAYS
7
292
36
194
24
29s
33
283
37
8
197
25
196
22
2s7
32
187
25
9
259
33
2s6
33
aso
43
368
39
10
lqDo
22
196
24
22~
25
286
3~t
11
173
21
87
is
310
33
341
38
12
189
22
202
24
2~Jo
29
267
28
216.7
26.S
181LS 2 ~ 7
~
a2~s
28a.7
~J.2
confirmation of Levine's [ 14] earlier reports of failure of interocular transfer in pigeons trained on a j u m p i n g stand. Furthermore, the failure of transfer between Stages 3 and 4 is inconsistent with Catania's [5,6] proposal that the subsequent change in posture following switching of eyecovers is responsible for the poor performance of the discrimination habit. During Stage 4, the pigeons were using the eye that they had already used on a large n u m b e r of trials during Stage 1 and were well accustomed to the apparatus. Nevertheless, contrary to what Catania might have predicted, these birds failed to learn the discrimination reversal in Stage 4 any faster than they had in Stage 3 using the other eye. I n d e e d , the performances in both these stages were highly similar and during the early portion of both stages, the pigeons jumped towards the previously positive stimulus a considerable n u m b e r of times before they began to jump to the correct platform. The results of the retention test administered between Stages 3 and 4 also indicate that in the jumping stand
situation there is no evidence for interocular transfer in the pigeon. When tested with the eye that had been uncovered during Stage l, the pigeons jumped towards the stimulus that had been negative during Stage 3, even though they had not been trained with that eye for an average of I 120 trials. In fact, in the last 660 of those trials, they had been trained with the other eye not to jump towards that stimulus, but towards the other one. It could be argued that the pigeons had simply learned a conditional discrimination, jumping to either stimulus depending on which eye was uncovered. Certainly both Catania [6] and Konnerman [13] have demonstrated that it is possible to train birds on conflicting discriminations using each eye separately in situations where there is normally good interocular transfer. However, Catania alternated the training sessions for each eye from day to day, whereas in the present experiment the pigeons were trained to criterion on one eye before being switched to the other. Konnerman failed to establish conflicting discriminations in domestic geese when one eye was trained to criterion first, even though he was able to do so when the geese were given alternate sessions for the left and fight eyes in the same day. This suggests that the pigeons' behaviour in the interpolated retention test of the present experiment was not the result of having learned a conditional and conflicting discrimination, but was a reflection of the absence of interocular transfer in the situation. Catania [6] suggested that one reason why he found transfer and Levine did not could be the difference in the number of responses required f o r learning in their respective training situations. Since Catania required his pigeons to make many thousands of responses, the resultant overtraining may have been responsible for the successful transfer from one eye to the other. However, the n u m b e r of trials to criterion required in "each stage of the present experiment was quite comparable to the number of responses made by pigeons in Meier's experiments [17] where he found transfer on both colour and pattern discriminations using a two-choice operant procedure. In our own laboratory, pigeons monocularly trained on a colour discrimination in a two-choice operant procedure show good interocular transfer in a training and testing paradigm identical to that used on the j u m p i n g stand even though the total n u m b e r of responses made in the key-pecking task was much less (Graves and Goodale, unpublished observations). The reasons for the absence or presence of interocular transfer in different situations are not at all clear. A n u m b e r of investigators have observed failure of transfer in birds trained on tasks other than jumping stands. Using an appetitive task in which pigeons had to approach the stimuli from some distance, Beritov and Chichinadze [3,7] found no evidence for interocular transfer of either colour or pattern discriminations. Zeie]: [26] found that chicks which had been monocularly habituated to the deep side of a visual cliff, showed depth avoidance when tested with the naive eye, but not with the trained eye. Similarly, Benowitz [1,2] has reported that although a monocularly learned suppression of pecking at distasteful objects did show good transfer in chickens, the extinction of the suppression did not. Ingle [ 12] has observed in the goldfish that a simple line orientation discrimination showed interocular transfer whereas a more difficult one did not. Indeed, in both fish and birds, the information transferred to the untrained eye frequently seems to be less complete than. that available to
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the trained eye. Thus both chickens and carp failed to show transfer of shape discriminations when the stimuli were altered from the original, even though they could discriminate the altered shapes with the trained eye [ 18,22]. Under certain training conditions, mammals with visual projections that are highly crossed such as the rabbit and the rat have shown very poor interocular transfer [8, 23-25]. It is evident from these and other experiments that there are probably a number of different factors affecting interocular transfer including exposure time, task difficulty, and the presence of irrelevant stimuli in the visual field of the untrained eye [ 12,20]. But it is difficult to see how any of these factors would easily explain the difference in interocular transfer found between pigeons trained on a jumping stand and those in a Skinner box. However, one probable difference between the two situations lies in the parts of the visual system used by the pigeon in each case; a distinction anticipated much earlier by Levine [151 and restated by Catania [ 4 - 6 1 in a different explanatory context. In the jumping stand, the pigeons were some distance from the dtscriminanda, approximately 15 cm (from the upright stimulus but less for the horizontal) and may therefore have used the lateral visual field to inspect the stimulus array since they are laterally far sighted. In the Skinner box, however, since the
birds were much closer to the stimulus keys and were also directing pecks at these keys, they were perhaps more likely to use that part of the visual field which in normal circumstances is binocularly represented. The lateral visual fields in an animal with panoramic vision, such as the pigeon, would represent two very different views of the world. Therefore, it might be expected that if only one of these fields included stimuli which were controlling behaviour, then some sort of selective attention by either unilateral suppression and/or emphasis of input could be operating. Certainly there is electrophysiological evidence for the existence of a commissural inhibitory mechanism in the optic tectum of the pigeon [21 ] and several mammalian species [10]. The failure of transfer in the jumping stand could therefore be a reflection of the operation of such inhibitory circuits. In contrast, the processing of visual information falling on those parts of the visual field which are binocularly represented would not be expected to require the participation of selective attention mechanisms. Consequently discriminative stimuli which are presented to this part of the visual field of one eye might show good interocular transfer to the other. However, this line of reasoning remains highly speculative until there is direct cine film or videotape analysis of the scanning and visual search patterns of pigeons in each of these situations.
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