The contribution of the rewarded and unrewarded stimulus in two-choice pattern discrimination in the rabbit

Behavioural Brain Research, 11 (1984) 135-143 Elsevier

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THE CONTRIBUTION OF THE REWARDED AND U N R E W A R D E D S T I M U L U S IN TWO-CHOICE PATTERN DISCRIMINATION IN THE RABBIT

M.W. VAN H O F and J. VAN HOF-VAN D U I N

Department of Physiology I, Erasmus Universiteit Rotterdam, P.O. Box 1738, 3000 DR Rotterdam (The Netherlands) (Received June 7th, 1983) (Revised version received October 3rd, 1983) (Accepted October 4th, 1983)

Key words: pattern discrimination - visual system - reward - rabbit

Rabbits were trained to discriminate vertical vs horizontal striations. After reaching criterion one of the patterns was randomly replaced by striations oriented at 135 °. Other rabbits were trained to discriminate 45 ° vs 135 ° striations. After reaching criterion, one of the patterns was randomly replaced by vertical or horizontal striations. It was found that performance remained at the 90 % correct level when the unrewarded pattern was present. When this was not the case performance dropped to 60-70 % correct. It was concluded that in the discrimination apparatus used in this study, the rabbit's choice is mainly controlled by the unrewarded stimulus.

INTRODUCTION

Several investigators have studied the role of the rewarded and unrewarded stimulus in twochoice pattern discrimination. Random replacement of one of the stimuli by a meaningless pattern is one of the methods which have been used 3. During two-choice pattern discrimination in the rabbit random replacement of the unrewarded pattern by a blank window disrupts performance more than replacement of the rewarded pattern 8. From this it may not be inferred that the animal's choice is mainly controlled by the negative stimulus. Matching a blank window with a striated pattern unbalances the amount of contrast and overall luminance of the two stimuli. Any innate preference for the brighter or non-striated target could give a similar result. With respect to the design of future experiments on the rabbit's visual system we decided to study 0166-4328/84/$03.00 © 1984 Elsevier Science Publishers B.V.

this problem in greater detail. The method was such that luminance and amount of contrast were matched in all pattern combinations used. METHOD

Animals Fifty-five chinchilla rabbits were used. Apparatus The pattern discrimination apparatus and the automatic control system have been described elsewhere8"7. The apparatus essentially consisted of a box with one wall having two hinged panels on which visual patterns could be back-projected. To make a correct choice, the animal was required to press the panel illuminated by the correct pattern. This response was automatically rewarded by a food pellet. Responding to the panel with the incorrect pattern produced no reward but it terminated the trial, as a non-correction proce-

136 dure was used. A 6 s intertrial interval was used throughout all training sessions. The patterns were projected on a 10 cm diameter circular window in which each panel was covered by glass and Kodatrace foil. The patterns were composed of white striations with a width of 1 cm on a dark background. Procedure The shaping procedure has been described before m'4. In all cases 100 trials were given per day. Thirty-five rabbits were trained to discriminate vertical vs horizontal striations (groups A 1 and A2). After reaching the 90 ~o correct level the rewarded or unrewarded pattern was randomly replaced by striations oriented at 135 ° . In 20 other rabbits (groups B, and B2) training began with 45 ° vs 135 ° striations. After the 90 ~o correct level had been reached one pattern was randomly

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replaced by v e r t i c a l o r horizontai striations, i hc full training procedure will be discussed in O-~c Results section. RESULTS

The procedure followed in group A l is illustrated in Fig. 1. Fifteen rabbits were trained to discriminate vertical vs horizontal striations (Fig. 1, phase I). One hundred trials were given with the rewarded pattern randomly left or right. All animals reached the 90 ":~ correct level in 2--6 days of training (average number of errors 55.13 (SE + 8.96). After this the rewarded or the unrewarded pattern was randomly replaced by a grating oriented at 135 °. Fig. 1, phase 1I shows the 4 pattern combinations which emerged. The animals were trained with these patterns for 5 consecutive days. The results obtained in phase II a r e / G

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Fig. 1. Group A,, n = 15, t00 trials per day. Phase I, vertical vs horizontal striations [vertical rewarded); phase II, one pattern randomly replaced by 135 ° striations. Five days of training; phase III. 45 ° vs 135 ° striations (45 ° rewarded); and phase IV. positive and negative patterns of phase I and III interchanged. Five days of training.

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shown in the left graph of Fig. 2. In the 50 trials in which the rewarded pattern had been replaced

sentially the same as that in group A 1. The only difference was that the horizontal striations were

(pattern combinations 3 and 4 phase II, Fig. 1) the percentage of correct choices remained at the 90 ~o level. The scores reached with the pattern combinations in which the unrewarded patterns had been replaced (1 and 2) were at the 60-70 ~o level. In phase III (Fig. 1) training was continued with oblique striations (45 ° rewarded). All animals reached the 90 % correct level in 2-5 days (average errors to criterion 112.00 (SE + 10.31). In phase IV (Fig. 1) the positive and negative patterns of phase I and III were combined during 5 consecutive days. Combinations 1 and 2 were the same as those in phase II but now the 135 ° striations were no longer meaningless. As the right graph of Fig. 2 shows, the scores with 1-2 were at the 90 ~o level. As could be expected the same was the case with the combination of the negative pattern of phase I and the positive pattern of phase III 3'4. The procedure followed in group A2 was es-

rewarded in phase I (Fig. 3). All 20 animals reached the 90 ~o correct level in 2-8 days (average number of errors 125.45, SE _+ 14.55). As in group A 1 the rewarded and unrewarded pattern was randomly replaced by 135 ° striations in phase II. Just as in group A2 only the pattern pairs which carried the negative pattern of phase I gave scores at the 90 ~o level (3-4 in the left graph of Fig. 4). In phase III the animals were trained with 45 ° vs 135 ° striations (45 ° rewarded). Criterion was reached in 3-6 days (errors to criterion 126.70, SE + 10.23). In phase IV the positive and negative patterns of phase I and Ill were combined during 5 consecutive days. As the right graph of Fig. 4 shows the scores of 1-2 and 3-4 were above 90 % correct. The results obtained with animals which started with 45 ° vs 135 ° striations in phase I (group B1, Figs. 5 and 6, group B 2, Figs. 7 and 8) were essentially the same. Random replacement of the rewarded or unrewarded pattern in phase II by 1-2

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Fig. 3. Group A z, n = 20, 100 trials per day. Phase I. horizontal vs vertical striations (horizontal rewardedl; phase I1. one pattern randomly replaced by 135 ° striations. Five days of training; phase III. 45 o vs 135 ° striations 145 ' rewarded): and phase IV. positive and negative patterns of phase I and III interchanged. Five days of training.

horizontal striations (Fig. 5) or vertical ones (Fig. 7) disrupted performance when the positive pattern was combined with the neutral one (1-2 in the left graphs of Figs. 6 and 8). In phase III (Figs. 5 and 7) training was continued with vertical and horizontal striations (vertical rewarded in Fig. 5 and horizontal rewarded in Fig. 7). The combinations of the positive pattern of phase I and III in phase IV gave 90 % scores in both groups (right graphs in Figs. 6 and 8). The results obtained in all groups show that 90 % level scores are only reached when a pattern is present which the animal has been trained to avoid. DISCUSSION

Several animals were watched during the discrimination process in phase II. In general they

had a tendency to approach one of the gates, with the nose pointing into the direction of the target 1°. No systematic preference for one side was seen. If the pattern, closest to the animal's head, happened to be the unrewarded one, they usually moved to the other target. Most errors were made when the head was closest to the meaningless pattern. In that situation the animals had a tendency to open that gate without inspecting the other one. In other words, in this particular discrimination apparatus, the decision is based on the position of the unrewarded pattern. The relative importance of the rewarded and unrewarded stimulus in discrimination learning has been studied in a number of species under a variety of training conditions 3. The results obtained in rats vary. Sutherland found that rats trained to discriminate between horizontal and vertical rectangles learned both to approach the

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positive pattern and to avoid the negative one 5. With open and closed shapes, in the same apparatus, rats learned to approach the positive shape rather than to avoid the negative one 6. Stevens and Fechter 4 found that rats trained with positive reinforcement showed more avoidance of the negative stimulus than approach of the positive one. However, the opposite was found for negatively reinforced rats. This suggests that the results described in the present report depend on the training conditions and are not necessarily specific for the rabbit. In a previous study TM it was described that rabbits have great difficulties with a "same-difference" discrimination. If both patterns were identical (horizontal-horizontal or vertical-vertical) opening of the left door was rewarded; if they were unidentical (vertical-horizontal or horizontal-vertical) the right door had to be opened. Only 7 out of 18 animals were able to learn this task. As the present results show, the rabbit has a tendency to make its decision on the basis of only

one of the patterns. This strategy is adequate for successful discrimination between a rewarded and an unrewarded pattern. A "same-difference" discrimination, on the other hand, requires a comparison of both patterns. In previous studies 12 rabbits were trained to discriminate vertical from horizontal striations binocularly. After reaching criterion training was continued monocularly, each eye receiving 100 presentations of the same patterns per day. It was found that in approximately one third of the animals performance differed considerably between the two eyes. A satisfactory explanation of this phenomenon has never been given. One of the speculations made in the discussion of the paper in which this "occular dominance" was described 12 was that rabbits with one eye occluded, in order to make a correct choice, have to develop a motor strategy which enables them to compare the patterns. In order to make the notion of motor strategy more specific it would be of interest to study whether the phenomenon of the dominant

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Fig. 5. Group Bt, n = 10. 100 trials per day. Phase I. 45 ~ vs t35 c (45 ° rewarded); phase II. one pattern randomly replaced by horizontal striations. Five days of training. Phase III. vertical vs horizontal striations (vertical rewarded); and phase IV, positive and negative patterns of phase 1 and III interchanged. Five days of training.

role of the unrewarded stimulus is also present in monocular pattern discrimination. If this would be the case one could argue that in many trials, due to the occlusion of one of the laterally implanted eyes, the open eye will be exposed to one pattern only. Suppose that the left eye is occluded and the animal sees the negative pattern only, it has to move to the left in order to find the rewarded pattern. In a similar situation with the right eye occluded it has to go to the right. Therefore "ocular dominance" could be due to either an inability to learn opposing motor strategies or an inability to identify the negative pattern with the two eyes separately. One method of eliminating motor strategies is a G O - N O G O discrimination. In that situation identification of the negative

pattern will be sufficient to reach high performance levels and no left-right strategies are needed. Up till now no G O - N O G O experiments in rabbits have been reported. Preliminary tests in 6 rabbits (I.S. Russell, personal communication) have shown that it is possible to train rabbits in a G O - N O G O situation. Rabbits show tittle interocular transfer 9 ' 13 •13-. If future experiments on monocular discrimination confm"n the dominant role of the negative stimulus, it would be worthwhile to consider the possibility of conflicting motor strategies as an explanation of the low level of interocular transfer. After a unilateral ablation o f the occipital lobe rabbits easily relearn to discriminate striated patterns with the eye contralateral to the intact hemi-

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Fig. 7. Group B 2 , I1 = 10, 100 trials per day. Phase 1, 45 ° vs 135 ° striations (45 ° rewarded); phase II, one pattern randomly replaced by vertical striations. Five days of training; phase III, horizontal vs vertical striations (horizontal rewarded); and phase IV, positive and negative patterns of phase I and Ill interchanged. Five days of training.

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sphere. With the eye contralateral to the lesion considerable retraining is necessary in order to reach the 90 % correct criterion ~I. Discrimination with the eye contralateral to the lesion is mediated by the ipsilateral cortical projection which corresponds to a narrow section of the visual field 1, In future experiments it will be studied whether the animal finally learns to discriminate the pattern by developing a complicated scanning technique and/or by learning to use the rewarded pattern in making its choice. ACKNOWLEDGMENTS

The authors are greatly indebted to Miss I. de Bloois, Mr. B.L.F: Weijer and:Mr, H, Dronk for their technical assistance.

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8 REFERENCES 1 De Vos-Korthals, W.H. and Van Hof, M.W., Pattern discrimination after unilateral and bilateral ablation of

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the occipital lobe in the rabbit, Behav. Brain Res.. 2 (1981) 219-222. De Vos-Korthals, W.H. and Van Hof, M.W., Interocular transfer in the rabbit tested without uninterrupted series of monocular trials, Behav. BrainRes., 9 (1983) 105-110. Mackintosh, N.J., The Psychology of Animal Learning, Academic Press, New York, 1974~ pp. 565~570. Stevens. D.A. and Fechter, L.D., Relative strengths of approach and avoidance tendencies in discrimination learning of rats trained under two types of reinforcement. J. Exp. Psychol., 76 (1968) 489-491. Sutherland' N" S" Visual discrirehnati°n ° f h°riz°ntal and vertical rectangles by rats on a new discrimination training apparatus, Quart. J. Exp. Psychol.. 13 (196t) 117-121. Sutherland, N S , Carr, A.E. and Mackintosh. J.A., Visual discrimination of open and closed shapes by rats. I, Quart. J. Exp. Psychol., 14 (1962) 129-I39. 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. Blot. Med.. 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.. Interocular transfer in the rabbit. Exp. Neurol.. 26 (1970) 103-108.

143 10 Van Hof, M.W. and Lagers-van Haselen, G.C., The retinal fixation area in the rabbit, Exp. Neurol., 41 (1973) 218-221. 11 Van Hof, M.W. and Lagers-van Haselen, G.C., Monocular pattern discrimination in rabbits after unilateral ablation of the visual cortex. Exp. Neurol., 46 (1975) 257-259. 12 Van Hof, M.W. and Van der Mark, F., Monocular pattern discrimination in normal and monocularly light-deprived rabbits, Physiol. Behav., 16 (1976) 775-781.

13 Van Hof, M.W. and Van der Mark, F., A quantitative study on interocular transfer in the rabbit, Physiol. Behav., 16 (1976) 715-717. 14 Van Hof, M.W. and Russell, I.S., Binocular vision in the rabbit, Physiol. Behav., 19 (1977) 121-128. 15 Van Hof, M.W., Interocular transfer and interhemispheric communication in the rabbit, In I. Steele Russell, M.W. van Hof, G. Berlucchi (Eds.), Structure and Functions of cerebral Commissures, MacMillan Press Ltd., 1979, pp. 224--235.