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Potentiation instead of overshadowing in the pigeon
BEHAVIORAL A N D N E U R A L BIOLOGY 2 5 , 18--29
(1979)
Potentiation Instead of Overshadowing in the Pigeon J. C. CLARKE, R. F. WESTBROOK, AND J. IRWIN 1 University of New South Wales, P. O. Box 1, Kensington, Sydney, N.S.W. 2033, Australia Experiment 1 provided an examination of the relative strengths of lithium chloride-based (10 mg/kg .3 M LiCI) visual and taste aversions in the pigeon. When conditioned separately taste aversions were stronger than visual aversions. When conditioned in compound, the strong taste cue potentiated rather than overshadowed the weak visual cue. Experiment 2 provided a replication of this potentiation of a weak visual cue by a strong taste cue. These results obtained with the pigeon parallel those recently reported with the rat where a strong taste potentiated rather than overshadowed a weak odor cue. The implications of these findings for theories of poison-based compound conditioning were discussed in terms of the relevance of the nontaste stimuli in a species" feeding behavior.
Rats readily learn aversions to substances on the basis of their gustatory characteristics (Garcia, Clarke, & Hankins, 1973); rats with difficulty learn aversions to substances on the basis of their visual characteristics (Best, Best, & Mickley, 1973); finally, rats will show overshadowing of visual by gustatory characteristics when both are followed by toxicosis (Garcia & Koelling, 1966). These and other results, e.g., from so-called cue-to-consequence studies (Garcia, McGowan, & Green, 1972), have encouraged an evolutionary based approach to food selection that relates the preferential associability of gustatory cues with toxicosis to the rat's structural development and ecological niche (e.g., Seligman & Hager, 1972). Specifically, such an approach treats the above results by (a) contrasting the rat's highly developed gustatory system with its poorly developed visual system and (b) linking such anatomical features to the rat's omnivorous, nocturnal feeding patterns. 1 This research was supported by Australian Research Grants Committee ARGC A76/ 15714. The authors are grateful to Mr. I. Faulks for his assistance with data collection. Experiment 1 was reported by J. hwin in a thesis submitted to University of New South Wales in partial fulfilment of the requirements for a B.Sc. Reprint requests should be sent to either of the first two authors at: School of Psychology, University of New South Wales, P. O. Box 1, Kensington, Sydney, N.S.W. 2033, Australia. 18
0163-1047/79/010018-12502.00/0 Copyright © 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
POTENTIATION IN THE PIGEON
19
This approach to food selection anticipates a different set of outcomes from the study of poison-based aversions in birds. The combination, in most birds, of a superior visual and rudimentary taste system together with their selective, diurnal feeding patterns suggests that birds will (a) readily learn aversions to substances on the basis of their visual characteristics, (b) with difficulty learn aversions to substances on the basis of their gustatory characteristics, and (c) show overshadowing of gustatory by visual characteristics when both are followed by toxicosis. There is considerable support for the first of these predictions: When ingestion was followed by toxicosis, chickens (Gaston, 1977; Martin, Bellingham, & Storlien, 1977) and quail (Czaplicki, Borrebach, & Wilcoxon, 1976; Wilcoxon, 1977) developed visual aversions. The second and third of these predictions, however, have received very little attention: There is, in fact, only one study (Wilcoxon, Dragoin, & Kral, 1971) on one species (quail) directed toward the relative associabilities of gustatory and visual stimuli with toxicosis in birds. That study is generally interpreted (e.g., Mackintosh, 1974, p. 55) to have confirmed these predictions: namely, that, although quail could learn taste aversions, such aversions were weak and could be overshadowed by the stronger visual aversions. However, there are several problems with the study of Wilcoxon e t al. (1971) that render such conclusions premature. First, this study has been criticized (Bittermam 1976) on the grounds that it did not include nonassociative control groups. Although such groups were employed in subsequent demonstrations of visual aversions in quail (Wilcoxon, 1977), the contribution of nonassociative factors to the relative strengths of visual and gustatory aversions remains to be determined. Second, assertions about overshadowing imply comparisons between groups. In the study of Wilcoxon et al., such comparisons were not drawn: All of the comparisons in that study were within-group pretest to post-test differences. Finally, the significance of any comparison in that study was obscured by the fact that such comparisons were drawn using multiple t tests without any control for inflation of the Type 1 error rate which such a procedure incurs (Hays, 1974, p. 593). In view of the theoretical importance accorded the study of Wilcoxon e t al. and in view of the interpretive problems which beset that study, the present experiments undertook with another avian species, the pigeon, a conceptual replication of the Wilcoxon et al. study. EXPERIMENT 1
Experiment 1 constitutes an examination of the relative associabilities of visual and gustatory CSs with a toxic US in the pigeon. Specifically, we sought to determine (a) if visual and gustatory aversions could be developed in the pigeon, (b) if visual aversions were stronger than gustatory aversions, (c) if visual aversions could overshadow gustatory aversions,
20
CLARKE, WESTBROOK, AND IRWIN
and (d) if these aversions were associative in nature (i.e., stronger than those observed in two control groups given neither the colored nor the tasty solution prior to poisoning and on the extinction trials, tested on either the colored or the tasty solution; had the aversions observed in these control groups turned out to be equal to those found in the pairing groups, then the operation of nonassociative rather than conditioning processes would have to have been assumed).
Method Subjects and apparatus. The subjects were 48 male experimentally naive hybrid pigeons weighing between 300 and 600 g at the start of training. They were individually housed in 42 x 42 x 22-cm wire cages where training and testing took place. Three clear plastic cups were affixed at floor level to the outside of a cage. The diameter of a cup was 7 cm and its depth was 6 cm. Mixed grain was available ad libitum in the center cup. The outside cups which contained the fluids were spaced 15 cm apart, center to center. Procedure. The pigeons were maintained on a 23,5-hr fluid-deprivation schedule. When daily fluid consumption of tap water had stabilized, the pigeons were randomly assigned to six groups (n = 8 per group). On 2 successive days, the pigeons were exposed during the 30-rain access period to the solution which they would subsequently encounter in the post-tests, either blue water or salty water, in an attempt to eliminate any neophobic effects (Barnett, 1963). Four more days of access to tap water intervened before acquisition. The six groups in the first experiment were C:C, T:T, CT:C, CT:T, W:C, and W:T (C = colored water; T = tasty water; W = tap water). The letter(s) before the colon refer(s) to the fluid(s) paired with poison (10 mg/kg .3 M lithium chloride intraorally infused after 30-min access to the acquisition fluid). The letter after the colon refers to the fluid presented on the extinction trials with tap water as the other alternative. Thus, group C:C refers to the pigeons poisoned after consuming a blue solution (. 1%, v/v, of McCormick's food coloring in tap water) and on the extinction trials given a choice between blue water and tap water. T:T refers to the pigeons poisoned after consuming a salty solution (. 12 M solution of sodium chloride) and on the extinction trials given a choice between salty water and tap water. CT:C refers to the pigeons poisoned after consuming a solution of b l u e , s a l t y water and on the extinction trials given a choice between blue water and tap water, etc. Two hours after administration of the toxin and for the next 7 days the pigeons were allowed continuous access to tap water. A further 5 days intervened between the acquisition day and the extinction days during which time the pigeons were readjusted to the 23.5-hr fluid-deprivation schedule. As indicated above, T:T, CT:T, and W:T then received two 30-min choice tests between salty flavored water and tap water; groups
21
P O T E N T I A T I O N IN T H E P I G E O N
C:C, CT:C, and W:C received two 30-min choice tests between blue colored water and tap water. Two days of plain water intervened between the choice tests. The positions of the target solution and of tap water were reversed on the second choice test. Results and Discussion The toxin produced signs of illness (enhanced fluid consumption, diarrhea, shivering, and some vomiting) in the birds. The data of principal interest are the preference ratios from the tests. These are the amount of the target solution, either salty flavored water or blue colored water, consumed across the 1-hr testing period divided by the total amount of fluid consumed in this period. Thus, a ratio of 1.0 indicates a complete preference for the target solution and a ratio of 0 indicates a complete aversion for that solution. Figure 1 shows the mean preference ratios for each of the groups. To z
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FIG. 1. Preference on extinction trials for either" a colored or tasty solution with tap water as the other alternative. Letters before the colon refer to the fluid(s) paired once with poisoning. Those after the colon refer to the fluid presented on the extinction trials (C = colored water; T = tasty water; W = tap water; CT = colored-tasty water). Thus CT:C designates the group poisoned after drinking the colored-tasty solution and, on the extinction trials, given a choice between colored water and tap water, etc.
22
CLARKE, WESTBROOK, AND IRWIN
test for the significance of any difference in preference ratios, a set o f planned nonorthogonal contrasts were written and analyzed according to the Bonferroni technique (Miller, 1966). With the significance level set at .05, 6 contrasts, and 1, 42 df, freedom, the critical F value was 7.71. It can be seen from the figure that both of the taste groups, groups CT:T and T:T, drank considerably less of the target solution than their appropriate controls, group W:T. This demonstrates (a) that gustatory aversions were developed which (b) were due to conditioning. This was confirmed by the statistical analysis which showed a significant difference between the control group ( W : T ) a n d the average of the taste experimental groups (CT:T and T:T), F (1,42) = 8.89, M S E = .45. Further, it can be seen from the figure that there were no differences in the amounts consumed of the target solution by the two taste experimental groups (CT:T and T:T), F < 1. This indicates that the presence of a color on conditioning day had not detracted from the strength of the taste aversion in group CT:T and implies that, in the pigeon, color cues are weak by comparison with taste cues and do not attenuate the associative strength of the stronger taste cue. Such an assertion about relatively strong taste and relatively weak color aversions is obvious from an inspection of the amounts consumed of their target solutions by groups T:T and C:C and confirmed by statistical analysis, F (1, 42) = 17.12, M S E = .86. The failure to produce any color aversion in group C:C is surprising; even more surprising, however, is the strong color aversion observed in group CT:C. The failure to observe a color aversion in the former group accounts for the overall failure to demonstrate color conditioning: Group W:C did not differ significantly from the average of groups C:C and CT:C, F (I, 42) = 2.21, M S E = . 111. However, the surprising difference between groups C:C and CT:C was confirmed statistically, F (1, 42) = 28.3, M S E = 1.42. Finally, although taste aversions were stronger than color aversion (groups T:T vs C:C) and although color did not detract from the strength of a taste aversion (groups CT:T vs T:T), there were no differences in the strengths of color and taste aversions after they had been conditioned in compound (groups CT:T vs CT:C), F < 1. The present results are surprising on three grounds. First, the relative strengths of gustatory and visual aversions in the pigeon are the opposite to those reported by Wilcoxon et al. (1971) in the quail. Second, the failure to observe any visual aversion in group C:C contrasts with several previous demonstrations of visual aversions in birds (Gaston, 1977; Martin et al., 1977; Czaplicki et al., 1976; Wilcoxon, 1977). Finally, the strong gustatory cue potentiated rather than overshadowed the weak visual cue. Since we have already assured ourselves (a) that taste aversions in the pigeon are stronger and occur over longer C S - U S intervals than visual aversions and (b) that the absence of a visual aversion in group C:C reflected the insensitivity of the testing procedure (R. F. W e s t b r o o k & J.
POTENTIATION 1N THE PIGEON
23
C. Clarke, unpublished data), Experiment 2 focused on the potentiation effect. EXPERIMENT 2
Overshadowing is a well-established principle in the literature on stimulus selection. It refers to the fact that a weak CS will acquire more associative strength if reinforced separately than if reinforced in compound with a strong CS (Pavlov, 1927). It has been obtained in a variety of conditioning procedures besides the original salivary preparation used by Pavlov: conditioned suppression of food-reinforced bar pressing (Kamin, 1969); conditioned suppression of kicking (Mackintosh, 1971); simultaneous discrimination tasks (D'Amato & Fazzaro, 1966); successive go/no-go discriminations (Miles & Jenkins, 1973); and, finally, poison-based aversions with rats (Revusky, 1971). It has also been claimed with quail (Wilcoxon et al., 1971). Although current theories of conditioning (e.g., Sutherland & Mackintosh, 1971, Rescorla & Wagner, 1972) differ in the precise way in which they embrace the facts of overshadowing, such theories share the assumption that there will be an inverse relationship between the conditioned strengths of the several components of a reinforced compound. Such an assumption, of course, cannot readily accommodate the results of Experiment 1 where a strong gustatory cue potentiated the otherwise weak visual cue. In view of the pervasiveness of overshadowing and in view of the theoretical importance it has justifiably attracted, we sought in Experiment 2 to replicate the potentiation finding. This experiment was designed along the same lines as the first but with the following modifications. First, the mode of drug administration selected was intraperitoneal instead of intraoral. The latter mode, if spillage is to be avoided, is time consuming and subsequent poison-based aversion studies in our laboratory (on long delay conditioning) revealed that intraperitoneal injections had the same effect as, were as safe as, and were much quicker and easier to administer than intraoral administration. Second, observations and filmed records of the pigeons' drinking styles revealed that some of the birds would plunge their heads into the drinking cups, close their eyes, and consume their daily ration of fluid in a minute or less. This raised the possibility that these birds may not have attended sufficiently to the color cues and, given the speed of their drinking, to the taste cues, either. Therefore, in Experiment 2 the drinking cups were replaced with glass calibrated cylinders. These forced a very much slower rate of drinking and prevented any contact with the fluid beyond the tip of the beak thus ensuring that the color of the fluid was always visible to the bird during consumption. Finally, another control group was added in Experiment 2. In the first experiment the control animals were given water on the poisoning day and either a blue or a salty solution on the extinction trials. This was done to assess the extent to which pigeons will
24
CLARKE, WESTBROOK, AND IRWIN
avoid a relatively novel substance following a poisoning episode even if that particular solution (blue or salty water) had not been paired with the poison. While the results of Experiment 1 indicate that a conditioned taste aversion was indeed produced, there still remains the possibility that the aversion to the blue water after compound conditioning (CT:C) was in fact an instance of cross-modal stimulus generalization and not potentiation. To investigate this possibility a control group was run in which the pigeons were poisoned after consuming the salty water and on the extinction trials given a choice between blue water and tap water.
Method Subjects and apparatus. The pigeons, their maintenance, and the apparatus were similar to those previously described (Experiment 1) except that calibrated cylinders were used instead of plastic cups. Above and to either side of the food cup, two glass 100-ml calibrated cylinders were also attached to the outside of the fi'ont wall. Their 0.5-cm-diameter glass spouts protruded into the cages for 4 cm. They were spaced 10 cm apart and were 10 cm from the floor of the cage. Procedure. The first 4 days were spent ensuring that all of the pigeons were drinking plain water flom the tubes. The pigeons were then randomly assigned to foul" groups (n = 19 per group) and administered two pretests. The pretests consisted of a 24-hr choice test between plain tap water and blue tap water followed by a further 24-hr choice test in which the positions of the plain and blue fluids were reversed. After 36 hr of fluid deprivation the control groups were allowed 20-min access to either plain tap water (group W:C) or salty flavored water (group T:C) and then given a 10 mg/kg ip injection of .3 M LiCI. The experimental groups were allowed 20-min access to either blue water (group C:C) or to blue-salty water (group CT:C) and then given the 10 mg/kg ip injection of .3 M LiCl. The blue colored and salty flavored solutions and the designations of the letters were as described in Experiment 1. Two hours after the injection the pigeons were allowed continuous access to plain water. Seven days later all pigeons were tested. The extinction tests were a 24-hr choice test between tap water and blue water and a second 24-hr choice test in which the positions of the plain and blue fluids were reversed. Results and Discussion All pigeons showed the symptoms of illness ah'eady described. The data of principal interest are the pretest and post-test preference ratios for the foul" groups. The mean preference ratios, which were calculated as in Experiment 1, are shown in Fig. 2. The pretest to post-test difference scores were analyzed by the technique of planned orthogonal contrasts (Hays, 1972, p. 581 ft.) with the significance level set at .05. It can be seen from the figure that the experimental groups (groups C:C and CT:C) drank
P O T E N T I A T I O N IN T H E PIGEON
25
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FIG. 2. Preference on extinction trials for colored water with tap water as the other alternative. Mean preconditioning c o n s u m p t i o n of the colored water is indicated on the e x t r e m e left o f the graph (see Fig. 1 for an explanation of the other details).
much less of the acquisition solution than the control groups (groups W:C and T:C). This was confirmed by the statistical analysis which demon: strated a significant difference between the average of the control groups (W:C and T:C) and the average of the experimental groups (C:C and CT:C), F (1, 72) = 9.29, MSE = .83. This indicates (a) that visual aversions were developed which (b) were due to conditioning. It can also be seen from the figure that there were no differences between the control groups (W:C and T:C), F = 1, demonstrating that the assertion about conditioning cannot be criticized on the grounds of an inadequate (group W:C) control group (Domjan, 1975). Finally, it can be seen from the figure that the pigeons conditioned to the compound (group CT:C) drank less of the blue water than did the pigeons (group C:C) conditioned and tested on the blue water. This replication of the potentiation effect observed in Experiment 1 was confirmed by the statistical analysis which showed a significant difference between groups CT:C and C:C, F (1, 72) = 6.46, M S E = .57. The potentiation effect, therefore, is sufficiently robust to withstand changes in testing procedure (1 hr in Experiment 1 versus 48 hr in Experiment 2) and in mode of administration of the toxin (intraoral in Experiment 1 versus intraperitoneal in Experiment 2).
26
CLARKE, WESTBROOK, AND IRWIN
GENERAL DISCUSSION Two findings emerge from the present experiments. First, when conditioned separately, taste aversions were stronger than color aversions. Second, color aversions were stronger when conditioned in compound than when conditioned separately. These findings are the opposite to those anticipated by an approach to food selection that relates the associabilities of cues with toxicosis to birds' structural development and ecological niche (Seligman & Hager, 1972). The present demonstration that taste aversions were stronger than visual aversions in a species with a highly developed visual system indicates that anatomical development per se provides little ground for anticipating which species will readily develop what aversions. Moreover, a structurally based approach fails to indicate why unmediated color aversions are strong in some avian species (e.g., chicks and quail) and weak in the pigeon and the buteo hawk (Brett, Hankins, & Garcia, 1976). Instead, the present findings indicate the need, at this stage, for a functional-behavioral approach to the formation of poison-based aversions. Specifically, such an approach must address: (a) the preferential associability of taste with toxicosis; (b) the facts of overshadowing; and (c) the major new finding observed here, the potentiation of a weak color cue by a strong taste cue. After poisoning, the pigeon is faced with the problem of identifying and, thereby, subsequently avoiding the cause of the illness. At least two properties of flavors and illness have been adduced to ensure that the substance which caused the illness will be identified on the basis of its flavor. First, there is a long history of an intimate and invariant relation between taste receptors, food ingestion, and postingestional consequences (cf. Rozin & Kalat, 1971). Second, the associability of taste and toxicosis may benefit from neurological links between taste and visceral receptors (cf. Garcia, McGowan, & Green, 1972). Thus, when the attributes of a substance compete for access to a toxin US, the flavor should overshadow the other attributes of that substance. Flavor-based avoidance, however, implies rejection after some contact with a potentially harmful substance. A more efficient avoidance strategy would involve identification, and thereby rejection, from a distance (cf. Brower, 1969). For the pigeon, visual cues provide the basis for distal identification. But, as the present results consistently show, visual avoidance is more profound when elaborated from a concomitant taste identification. Again it is possible to suggest an advantage here: In the absence of taste identification, the capacity for visual identification would leave the pigeon vulnerable to the formation of "superstitious" aversions between toxicosis and any immediately prior visual event. Thus, the pigeon must link the visual attributes of the ingested substance with the toxic consequences of consumption. And, it is reasonable to suppose, since the edible substance is identified by its taste, there must be some
POTENTIATION IN THE PIGEON
27
process by which the taste "marks "' and thereby potentiates the visual characteristics of the substance. In view of the importance of visual stimuli in the pigeon's search for food, it is perhaps not surprising that taste marks the visual characteristics of the ingested substance. Although it still remains to be determined in the pigeon, it seems unlikely that other attributes of an ingested substance, e.g., odor, would be similarly marked. The rat, in sharp contrast to the pigeon, does rely on olfactory stimuli in the distal location and identification of focd. Thus, for the rat, taste should overshadow visual stimuli and potentiate olfactory stimuli. The former has considerable empirical support (e.g., Best, Best, & Henggeler, 1977) but the latter has only recently been confirmed. Rusiniak, Hankins, Garcia, & Brett (1979), in a paradigm similar to the one employed in the present experiments, found that odor was a weak and taste a strong cue for illness when either cue was conditioned separately. However, when other rats were given the tasty scented stimulus prior to toxicosis, strong odor conditioning was then obtained. These results nicely parallel those obtained in the pigeon but it will be important to determine and not assume the generality of these effects across various species: Specifically, such effects might be expected only in species that identify an edible substance primarily on the basis of its taste. Such effects might not occur, therefore, in precocial birds, e.g., chicks and quail, whose developmental maturity at birth may selectively and uniquely condition them toward the visual identification of an edible substance. Finally, we shall outline two approaches to the nature of the potentiation effect. The first assumes that tastes preferentially associate with illness and, therefore, that the taste overshadowed the visual cue in the present experiments. However, it also assumes that, prior to toxicosis, the visual cue had already associated with the taste US. By assigning a dual role to the taste as a US and a CS, the present account permits the visual cue, through its association with the now aversive taste, strong control over the pigeon"s avoidance. The potentiation of odor by taste in the rat, according to this account, encourages the further assumption that there are species differences in the ease with which cues associate with a taste US. The second account assumes the unique importance of certain stimuli in constituting, along with taste, the edible object. The spatiotemporal contiguity of, for example, blue-salty water will generate a representation of that object which, it is further assumed, will gain direct access to the illness. The taste, according to this account, does not potentiate or overshadow the color but, instead, forms the necessary basis for the pigeon developing a representation of an edible object and, thereby, associating that representation with illness. Whether potentiation can be related to the facts of overshadowing via
28
CLARKE, WESTBROOK, AND IRWIN
familiar principles or requires a relatively novel treatment in terms of the animal learning about objects remains to be determined.
REFERENCES Barnett, S. A. (1963). The Rat: A study in behavior. Chicago: Aldine. Best, P. J., Best, M. R., & Henggeler, S. (1977). The contribution of environmental non-ingestive cues in conditioning with aversive internal consequences. In L. M. Barker, M. R. Best, & M. Domjan (Eds.), Learning mechanisms in food selection. Waco, Tex.: Baylor Univ. Press. Bitterman, M. E. (1976). Flavor aversion studies, Science, 192, 266-267. Brett, L., Hankins, W. G., & Garcia, J. (1976). Prey-lithium aversions. III. Buteo hawks. Behavioral Biology, 17, 87-98. Brower, L. P. (1969). Ecological chemistry. Scientific American, 220, 22-29. Czaplicki, J. A , Borrebach, D. E., & Wilcoxon, H. C. (1976). Stimulus generalization of an illness-induced aversion to different intensities of colored water in Japanese quail. Animal Learning and Behavior, 4, 45-48. D'Amato, M. R., & Fazzaro, J. (1966). Attention and cue-producing behavior in the monkey. Journal of Experimental Analysis of Behavior, 9, 469-473. Domjan, M. (1975). Poison-induced neophobia in rats: Role of stimulus generalization of conditioned taste aversions. Animal Learning and Behavior, 3, 205-211. Domjan, M., & Wilson, N, E. (1972). Specificity of cue to consequence in aversion learning in the rat. Psychonomic Science, 26, 143-145. Garcia, J., Clarke, J. C., & Hankins, W. G. (1973). Natural responses to scheduled rewards. In P. P. G. Klopfer & P. H. Klopfer (Eds.), Perspectives in Ethology, Vol. 1. New York: Plenum. Garcia, J., & KoeIling, R. A. (1966). Relation of cue to consequence in avoidance learning. Psychonomic Science, 4, 123-124. Garcia, J., McGowan, B. K., & Green, K. F. (1972). Biological constraints on conditioning. In A. H. Black & W. F, Prokasy (Eds.), Classical conditioning. II: Current research and theory. New York: Appleton-Century-Crofts. Gaston, K. E. (1977). An illness-induced conditioned aversion in domestic chicks: One-trial learning with a long delay of reinforcement, Behavioral Biology, 20, 441-453. Hays, W. L. (1974). Statistics for the social sciences. New York: Holt, Rinehart & Winston. Kamin, L. J. (1969), Predictability, surprise, attention and conditioning. In B. A. Campbell & R. M. Church (Eds.). Punishment and aversive behavior. New York: AppletonCentury-Crofts. Mackintosh, N. J. (1971). An analysis of overshadowing and blocking. Quarterly Journal of Experimental Psychology, 23, 118-125. Mackintosh, N. J. (1974). The psychology and animal learning. New York: Academic Press. Martin, G. M., Bellingham, W. P., & Storlien, L. H. (1977). Physiology and Behavior, 18, 415-420. Miles, C. G., & Jenkins, H. M. (1973). Overshadowing in operant conditioning as a function of discriminability. Learning and Motivation. 4, 11-27. Miller, R. G. (1966). Simultaneous statistical inference. New York: McGraw-Hill. Pavlov, I. P. (1927). Conditioned reflexes. London: Oxford Univ. Press. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning. H: Current research and theory. New York: Appleton-Century -Crofts. Revusky, S. (1971), The role of interference in association over a delay. In W. K. Honig and P. H. R. James (Eds.), Animal memory. New York: Academic Press.
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Rozin, P., & Kalat, J. W. (1971). Specific hungers and poisoning as adaptive specializations of learning. Psychological Review, 78, 459-486. Rusiniak, K. W., Hankins, W. G., Garcia, J., & Brett, L. (1979). Flavor-illness aversions. I. Potentiation of odor by taste in rats. Behavioral and Neural Biology, 25, 1-17. Seligman, M. E. P., & Hager, J. L. (1972). Biological boundaries of learning. New York: Appleton-Century-Crofts. Sutherland, N. S., & Mackintosh, N. J. (1971). Mechanisms of animal discrimination •learning. New York: Academic Press. Wilcoxon, H. C. (1977). Learning of ingestive aversions in avian species. In L. M. Barker, M. R. Best, & M. Domjan (Eds.), Learning mechanisms in food selection, pp. 419-473. Waco, Tex.: Baylor Univ. Press. Wilcoxon, H. C., Dragoin, W. B., & Kral, D. A. (1971). Illness-induced aversions in rat and quail: Relative salience of visual and gustatory cues. Science, 171, 826-828.
(1979)
Potentiation Instead of Overshadowing in the Pigeon J. C. CLARKE, R. F. WESTBROOK, AND J. IRWIN 1 University of New South Wales, P. O. Box 1, Kensington, Sydney, N.S.W. 2033, Australia Experiment 1 provided an examination of the relative strengths of lithium chloride-based (10 mg/kg .3 M LiCI) visual and taste aversions in the pigeon. When conditioned separately taste aversions were stronger than visual aversions. When conditioned in compound, the strong taste cue potentiated rather than overshadowed the weak visual cue. Experiment 2 provided a replication of this potentiation of a weak visual cue by a strong taste cue. These results obtained with the pigeon parallel those recently reported with the rat where a strong taste potentiated rather than overshadowed a weak odor cue. The implications of these findings for theories of poison-based compound conditioning were discussed in terms of the relevance of the nontaste stimuli in a species" feeding behavior.
Rats readily learn aversions to substances on the basis of their gustatory characteristics (Garcia, Clarke, & Hankins, 1973); rats with difficulty learn aversions to substances on the basis of their visual characteristics (Best, Best, & Mickley, 1973); finally, rats will show overshadowing of visual by gustatory characteristics when both are followed by toxicosis (Garcia & Koelling, 1966). These and other results, e.g., from so-called cue-to-consequence studies (Garcia, McGowan, & Green, 1972), have encouraged an evolutionary based approach to food selection that relates the preferential associability of gustatory cues with toxicosis to the rat's structural development and ecological niche (e.g., Seligman & Hager, 1972). Specifically, such an approach treats the above results by (a) contrasting the rat's highly developed gustatory system with its poorly developed visual system and (b) linking such anatomical features to the rat's omnivorous, nocturnal feeding patterns. 1 This research was supported by Australian Research Grants Committee ARGC A76/ 15714. The authors are grateful to Mr. I. Faulks for his assistance with data collection. Experiment 1 was reported by J. hwin in a thesis submitted to University of New South Wales in partial fulfilment of the requirements for a B.Sc. Reprint requests should be sent to either of the first two authors at: School of Psychology, University of New South Wales, P. O. Box 1, Kensington, Sydney, N.S.W. 2033, Australia. 18
0163-1047/79/010018-12502.00/0 Copyright © 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.
POTENTIATION IN THE PIGEON
19
This approach to food selection anticipates a different set of outcomes from the study of poison-based aversions in birds. The combination, in most birds, of a superior visual and rudimentary taste system together with their selective, diurnal feeding patterns suggests that birds will (a) readily learn aversions to substances on the basis of their visual characteristics, (b) with difficulty learn aversions to substances on the basis of their gustatory characteristics, and (c) show overshadowing of gustatory by visual characteristics when both are followed by toxicosis. There is considerable support for the first of these predictions: When ingestion was followed by toxicosis, chickens (Gaston, 1977; Martin, Bellingham, & Storlien, 1977) and quail (Czaplicki, Borrebach, & Wilcoxon, 1976; Wilcoxon, 1977) developed visual aversions. The second and third of these predictions, however, have received very little attention: There is, in fact, only one study (Wilcoxon, Dragoin, & Kral, 1971) on one species (quail) directed toward the relative associabilities of gustatory and visual stimuli with toxicosis in birds. That study is generally interpreted (e.g., Mackintosh, 1974, p. 55) to have confirmed these predictions: namely, that, although quail could learn taste aversions, such aversions were weak and could be overshadowed by the stronger visual aversions. However, there are several problems with the study of Wilcoxon e t al. (1971) that render such conclusions premature. First, this study has been criticized (Bittermam 1976) on the grounds that it did not include nonassociative control groups. Although such groups were employed in subsequent demonstrations of visual aversions in quail (Wilcoxon, 1977), the contribution of nonassociative factors to the relative strengths of visual and gustatory aversions remains to be determined. Second, assertions about overshadowing imply comparisons between groups. In the study of Wilcoxon et al., such comparisons were not drawn: All of the comparisons in that study were within-group pretest to post-test differences. Finally, the significance of any comparison in that study was obscured by the fact that such comparisons were drawn using multiple t tests without any control for inflation of the Type 1 error rate which such a procedure incurs (Hays, 1974, p. 593). In view of the theoretical importance accorded the study of Wilcoxon e t al. and in view of the interpretive problems which beset that study, the present experiments undertook with another avian species, the pigeon, a conceptual replication of the Wilcoxon et al. study. EXPERIMENT 1
Experiment 1 constitutes an examination of the relative associabilities of visual and gustatory CSs with a toxic US in the pigeon. Specifically, we sought to determine (a) if visual and gustatory aversions could be developed in the pigeon, (b) if visual aversions were stronger than gustatory aversions, (c) if visual aversions could overshadow gustatory aversions,
20
CLARKE, WESTBROOK, AND IRWIN
and (d) if these aversions were associative in nature (i.e., stronger than those observed in two control groups given neither the colored nor the tasty solution prior to poisoning and on the extinction trials, tested on either the colored or the tasty solution; had the aversions observed in these control groups turned out to be equal to those found in the pairing groups, then the operation of nonassociative rather than conditioning processes would have to have been assumed).
Method Subjects and apparatus. The subjects were 48 male experimentally naive hybrid pigeons weighing between 300 and 600 g at the start of training. They were individually housed in 42 x 42 x 22-cm wire cages where training and testing took place. Three clear plastic cups were affixed at floor level to the outside of a cage. The diameter of a cup was 7 cm and its depth was 6 cm. Mixed grain was available ad libitum in the center cup. The outside cups which contained the fluids were spaced 15 cm apart, center to center. Procedure. The pigeons were maintained on a 23,5-hr fluid-deprivation schedule. When daily fluid consumption of tap water had stabilized, the pigeons were randomly assigned to six groups (n = 8 per group). On 2 successive days, the pigeons were exposed during the 30-rain access period to the solution which they would subsequently encounter in the post-tests, either blue water or salty water, in an attempt to eliminate any neophobic effects (Barnett, 1963). Four more days of access to tap water intervened before acquisition. The six groups in the first experiment were C:C, T:T, CT:C, CT:T, W:C, and W:T (C = colored water; T = tasty water; W = tap water). The letter(s) before the colon refer(s) to the fluid(s) paired with poison (10 mg/kg .3 M lithium chloride intraorally infused after 30-min access to the acquisition fluid). The letter after the colon refers to the fluid presented on the extinction trials with tap water as the other alternative. Thus, group C:C refers to the pigeons poisoned after consuming a blue solution (. 1%, v/v, of McCormick's food coloring in tap water) and on the extinction trials given a choice between blue water and tap water. T:T refers to the pigeons poisoned after consuming a salty solution (. 12 M solution of sodium chloride) and on the extinction trials given a choice between salty water and tap water. CT:C refers to the pigeons poisoned after consuming a solution of b l u e , s a l t y water and on the extinction trials given a choice between blue water and tap water, etc. Two hours after administration of the toxin and for the next 7 days the pigeons were allowed continuous access to tap water. A further 5 days intervened between the acquisition day and the extinction days during which time the pigeons were readjusted to the 23.5-hr fluid-deprivation schedule. As indicated above, T:T, CT:T, and W:T then received two 30-min choice tests between salty flavored water and tap water; groups
21
P O T E N T I A T I O N IN T H E P I G E O N
C:C, CT:C, and W:C received two 30-min choice tests between blue colored water and tap water. Two days of plain water intervened between the choice tests. The positions of the target solution and of tap water were reversed on the second choice test. Results and Discussion The toxin produced signs of illness (enhanced fluid consumption, diarrhea, shivering, and some vomiting) in the birds. The data of principal interest are the preference ratios from the tests. These are the amount of the target solution, either salty flavored water or blue colored water, consumed across the 1-hr testing period divided by the total amount of fluid consumed in this period. Thus, a ratio of 1.0 indicates a complete preference for the target solution and a ratio of 0 indicates a complete aversion for that solution. Figure 1 shows the mean preference ratios for each of the groups. To z
-0 I--
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FIG. 1. Preference on extinction trials for either" a colored or tasty solution with tap water as the other alternative. Letters before the colon refer to the fluid(s) paired once with poisoning. Those after the colon refer to the fluid presented on the extinction trials (C = colored water; T = tasty water; W = tap water; CT = colored-tasty water). Thus CT:C designates the group poisoned after drinking the colored-tasty solution and, on the extinction trials, given a choice between colored water and tap water, etc.
22
CLARKE, WESTBROOK, AND IRWIN
test for the significance of any difference in preference ratios, a set o f planned nonorthogonal contrasts were written and analyzed according to the Bonferroni technique (Miller, 1966). With the significance level set at .05, 6 contrasts, and 1, 42 df, freedom, the critical F value was 7.71. It can be seen from the figure that both of the taste groups, groups CT:T and T:T, drank considerably less of the target solution than their appropriate controls, group W:T. This demonstrates (a) that gustatory aversions were developed which (b) were due to conditioning. This was confirmed by the statistical analysis which showed a significant difference between the control group ( W : T ) a n d the average of the taste experimental groups (CT:T and T:T), F (1,42) = 8.89, M S E = .45. Further, it can be seen from the figure that there were no differences in the amounts consumed of the target solution by the two taste experimental groups (CT:T and T:T), F < 1. This indicates that the presence of a color on conditioning day had not detracted from the strength of the taste aversion in group CT:T and implies that, in the pigeon, color cues are weak by comparison with taste cues and do not attenuate the associative strength of the stronger taste cue. Such an assertion about relatively strong taste and relatively weak color aversions is obvious from an inspection of the amounts consumed of their target solutions by groups T:T and C:C and confirmed by statistical analysis, F (1, 42) = 17.12, M S E = .86. The failure to produce any color aversion in group C:C is surprising; even more surprising, however, is the strong color aversion observed in group CT:C. The failure to observe a color aversion in the former group accounts for the overall failure to demonstrate color conditioning: Group W:C did not differ significantly from the average of groups C:C and CT:C, F (I, 42) = 2.21, M S E = . 111. However, the surprising difference between groups C:C and CT:C was confirmed statistically, F (1, 42) = 28.3, M S E = 1.42. Finally, although taste aversions were stronger than color aversion (groups T:T vs C:C) and although color did not detract from the strength of a taste aversion (groups CT:T vs T:T), there were no differences in the strengths of color and taste aversions after they had been conditioned in compound (groups CT:T vs CT:C), F < 1. The present results are surprising on three grounds. First, the relative strengths of gustatory and visual aversions in the pigeon are the opposite to those reported by Wilcoxon et al. (1971) in the quail. Second, the failure to observe any visual aversion in group C:C contrasts with several previous demonstrations of visual aversions in birds (Gaston, 1977; Martin et al., 1977; Czaplicki et al., 1976; Wilcoxon, 1977). Finally, the strong gustatory cue potentiated rather than overshadowed the weak visual cue. Since we have already assured ourselves (a) that taste aversions in the pigeon are stronger and occur over longer C S - U S intervals than visual aversions and (b) that the absence of a visual aversion in group C:C reflected the insensitivity of the testing procedure (R. F. W e s t b r o o k & J.
POTENTIATION 1N THE PIGEON
23
C. Clarke, unpublished data), Experiment 2 focused on the potentiation effect. EXPERIMENT 2
Overshadowing is a well-established principle in the literature on stimulus selection. It refers to the fact that a weak CS will acquire more associative strength if reinforced separately than if reinforced in compound with a strong CS (Pavlov, 1927). It has been obtained in a variety of conditioning procedures besides the original salivary preparation used by Pavlov: conditioned suppression of food-reinforced bar pressing (Kamin, 1969); conditioned suppression of kicking (Mackintosh, 1971); simultaneous discrimination tasks (D'Amato & Fazzaro, 1966); successive go/no-go discriminations (Miles & Jenkins, 1973); and, finally, poison-based aversions with rats (Revusky, 1971). It has also been claimed with quail (Wilcoxon et al., 1971). Although current theories of conditioning (e.g., Sutherland & Mackintosh, 1971, Rescorla & Wagner, 1972) differ in the precise way in which they embrace the facts of overshadowing, such theories share the assumption that there will be an inverse relationship between the conditioned strengths of the several components of a reinforced compound. Such an assumption, of course, cannot readily accommodate the results of Experiment 1 where a strong gustatory cue potentiated the otherwise weak visual cue. In view of the pervasiveness of overshadowing and in view of the theoretical importance it has justifiably attracted, we sought in Experiment 2 to replicate the potentiation finding. This experiment was designed along the same lines as the first but with the following modifications. First, the mode of drug administration selected was intraperitoneal instead of intraoral. The latter mode, if spillage is to be avoided, is time consuming and subsequent poison-based aversion studies in our laboratory (on long delay conditioning) revealed that intraperitoneal injections had the same effect as, were as safe as, and were much quicker and easier to administer than intraoral administration. Second, observations and filmed records of the pigeons' drinking styles revealed that some of the birds would plunge their heads into the drinking cups, close their eyes, and consume their daily ration of fluid in a minute or less. This raised the possibility that these birds may not have attended sufficiently to the color cues and, given the speed of their drinking, to the taste cues, either. Therefore, in Experiment 2 the drinking cups were replaced with glass calibrated cylinders. These forced a very much slower rate of drinking and prevented any contact with the fluid beyond the tip of the beak thus ensuring that the color of the fluid was always visible to the bird during consumption. Finally, another control group was added in Experiment 2. In the first experiment the control animals were given water on the poisoning day and either a blue or a salty solution on the extinction trials. This was done to assess the extent to which pigeons will
24
CLARKE, WESTBROOK, AND IRWIN
avoid a relatively novel substance following a poisoning episode even if that particular solution (blue or salty water) had not been paired with the poison. While the results of Experiment 1 indicate that a conditioned taste aversion was indeed produced, there still remains the possibility that the aversion to the blue water after compound conditioning (CT:C) was in fact an instance of cross-modal stimulus generalization and not potentiation. To investigate this possibility a control group was run in which the pigeons were poisoned after consuming the salty water and on the extinction trials given a choice between blue water and tap water.
Method Subjects and apparatus. The pigeons, their maintenance, and the apparatus were similar to those previously described (Experiment 1) except that calibrated cylinders were used instead of plastic cups. Above and to either side of the food cup, two glass 100-ml calibrated cylinders were also attached to the outside of the fi'ont wall. Their 0.5-cm-diameter glass spouts protruded into the cages for 4 cm. They were spaced 10 cm apart and were 10 cm from the floor of the cage. Procedure. The first 4 days were spent ensuring that all of the pigeons were drinking plain water flom the tubes. The pigeons were then randomly assigned to foul" groups (n = 19 per group) and administered two pretests. The pretests consisted of a 24-hr choice test between plain tap water and blue tap water followed by a further 24-hr choice test in which the positions of the plain and blue fluids were reversed. After 36 hr of fluid deprivation the control groups were allowed 20-min access to either plain tap water (group W:C) or salty flavored water (group T:C) and then given a 10 mg/kg ip injection of .3 M LiCI. The experimental groups were allowed 20-min access to either blue water (group C:C) or to blue-salty water (group CT:C) and then given the 10 mg/kg ip injection of .3 M LiCl. The blue colored and salty flavored solutions and the designations of the letters were as described in Experiment 1. Two hours after the injection the pigeons were allowed continuous access to plain water. Seven days later all pigeons were tested. The extinction tests were a 24-hr choice test between tap water and blue water and a second 24-hr choice test in which the positions of the plain and blue fluids were reversed. Results and Discussion All pigeons showed the symptoms of illness ah'eady described. The data of principal interest are the pretest and post-test preference ratios for the foul" groups. The mean preference ratios, which were calculated as in Experiment 1, are shown in Fig. 2. The pretest to post-test difference scores were analyzed by the technique of planned orthogonal contrasts (Hays, 1972, p. 581 ft.) with the significance level set at .05. It can be seen from the figure that the experimental groups (groups C:C and CT:C) drank
P O T E N T I A T I O N IN T H E PIGEON
25
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FIG. 2. Preference on extinction trials for colored water with tap water as the other alternative. Mean preconditioning c o n s u m p t i o n of the colored water is indicated on the e x t r e m e left o f the graph (see Fig. 1 for an explanation of the other details).
much less of the acquisition solution than the control groups (groups W:C and T:C). This was confirmed by the statistical analysis which demon: strated a significant difference between the average of the control groups (W:C and T:C) and the average of the experimental groups (C:C and CT:C), F (1, 72) = 9.29, MSE = .83. This indicates (a) that visual aversions were developed which (b) were due to conditioning. It can also be seen from the figure that there were no differences between the control groups (W:C and T:C), F = 1, demonstrating that the assertion about conditioning cannot be criticized on the grounds of an inadequate (group W:C) control group (Domjan, 1975). Finally, it can be seen from the figure that the pigeons conditioned to the compound (group CT:C) drank less of the blue water than did the pigeons (group C:C) conditioned and tested on the blue water. This replication of the potentiation effect observed in Experiment 1 was confirmed by the statistical analysis which showed a significant difference between groups CT:C and C:C, F (1, 72) = 6.46, M S E = .57. The potentiation effect, therefore, is sufficiently robust to withstand changes in testing procedure (1 hr in Experiment 1 versus 48 hr in Experiment 2) and in mode of administration of the toxin (intraoral in Experiment 1 versus intraperitoneal in Experiment 2).
26
CLARKE, WESTBROOK, AND IRWIN
GENERAL DISCUSSION Two findings emerge from the present experiments. First, when conditioned separately, taste aversions were stronger than color aversions. Second, color aversions were stronger when conditioned in compound than when conditioned separately. These findings are the opposite to those anticipated by an approach to food selection that relates the associabilities of cues with toxicosis to birds' structural development and ecological niche (Seligman & Hager, 1972). The present demonstration that taste aversions were stronger than visual aversions in a species with a highly developed visual system indicates that anatomical development per se provides little ground for anticipating which species will readily develop what aversions. Moreover, a structurally based approach fails to indicate why unmediated color aversions are strong in some avian species (e.g., chicks and quail) and weak in the pigeon and the buteo hawk (Brett, Hankins, & Garcia, 1976). Instead, the present findings indicate the need, at this stage, for a functional-behavioral approach to the formation of poison-based aversions. Specifically, such an approach must address: (a) the preferential associability of taste with toxicosis; (b) the facts of overshadowing; and (c) the major new finding observed here, the potentiation of a weak color cue by a strong taste cue. After poisoning, the pigeon is faced with the problem of identifying and, thereby, subsequently avoiding the cause of the illness. At least two properties of flavors and illness have been adduced to ensure that the substance which caused the illness will be identified on the basis of its flavor. First, there is a long history of an intimate and invariant relation between taste receptors, food ingestion, and postingestional consequences (cf. Rozin & Kalat, 1971). Second, the associability of taste and toxicosis may benefit from neurological links between taste and visceral receptors (cf. Garcia, McGowan, & Green, 1972). Thus, when the attributes of a substance compete for access to a toxin US, the flavor should overshadow the other attributes of that substance. Flavor-based avoidance, however, implies rejection after some contact with a potentially harmful substance. A more efficient avoidance strategy would involve identification, and thereby rejection, from a distance (cf. Brower, 1969). For the pigeon, visual cues provide the basis for distal identification. But, as the present results consistently show, visual avoidance is more profound when elaborated from a concomitant taste identification. Again it is possible to suggest an advantage here: In the absence of taste identification, the capacity for visual identification would leave the pigeon vulnerable to the formation of "superstitious" aversions between toxicosis and any immediately prior visual event. Thus, the pigeon must link the visual attributes of the ingested substance with the toxic consequences of consumption. And, it is reasonable to suppose, since the edible substance is identified by its taste, there must be some
POTENTIATION IN THE PIGEON
27
process by which the taste "marks "' and thereby potentiates the visual characteristics of the substance. In view of the importance of visual stimuli in the pigeon's search for food, it is perhaps not surprising that taste marks the visual characteristics of the ingested substance. Although it still remains to be determined in the pigeon, it seems unlikely that other attributes of an ingested substance, e.g., odor, would be similarly marked. The rat, in sharp contrast to the pigeon, does rely on olfactory stimuli in the distal location and identification of focd. Thus, for the rat, taste should overshadow visual stimuli and potentiate olfactory stimuli. The former has considerable empirical support (e.g., Best, Best, & Henggeler, 1977) but the latter has only recently been confirmed. Rusiniak, Hankins, Garcia, & Brett (1979), in a paradigm similar to the one employed in the present experiments, found that odor was a weak and taste a strong cue for illness when either cue was conditioned separately. However, when other rats were given the tasty scented stimulus prior to toxicosis, strong odor conditioning was then obtained. These results nicely parallel those obtained in the pigeon but it will be important to determine and not assume the generality of these effects across various species: Specifically, such effects might be expected only in species that identify an edible substance primarily on the basis of its taste. Such effects might not occur, therefore, in precocial birds, e.g., chicks and quail, whose developmental maturity at birth may selectively and uniquely condition them toward the visual identification of an edible substance. Finally, we shall outline two approaches to the nature of the potentiation effect. The first assumes that tastes preferentially associate with illness and, therefore, that the taste overshadowed the visual cue in the present experiments. However, it also assumes that, prior to toxicosis, the visual cue had already associated with the taste US. By assigning a dual role to the taste as a US and a CS, the present account permits the visual cue, through its association with the now aversive taste, strong control over the pigeon"s avoidance. The potentiation of odor by taste in the rat, according to this account, encourages the further assumption that there are species differences in the ease with which cues associate with a taste US. The second account assumes the unique importance of certain stimuli in constituting, along with taste, the edible object. The spatiotemporal contiguity of, for example, blue-salty water will generate a representation of that object which, it is further assumed, will gain direct access to the illness. The taste, according to this account, does not potentiate or overshadow the color but, instead, forms the necessary basis for the pigeon developing a representation of an edible object and, thereby, associating that representation with illness. Whether potentiation can be related to the facts of overshadowing via
28
CLARKE, WESTBROOK, AND IRWIN
familiar principles or requires a relatively novel treatment in terms of the animal learning about objects remains to be determined.
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Rozin, P., & Kalat, J. W. (1971). Specific hungers and poisoning as adaptive specializations of learning. Psychological Review, 78, 459-486. Rusiniak, K. W., Hankins, W. G., Garcia, J., & Brett, L. (1979). Flavor-illness aversions. I. Potentiation of odor by taste in rats. Behavioral and Neural Biology, 25, 1-17. Seligman, M. E. P., & Hager, J. L. (1972). Biological boundaries of learning. New York: Appleton-Century-Crofts. Sutherland, N. S., & Mackintosh, N. J. (1971). Mechanisms of animal discrimination •learning. New York: Academic Press. Wilcoxon, H. C. (1977). Learning of ingestive aversions in avian species. In L. M. Barker, M. R. Best, & M. Domjan (Eds.), Learning mechanisms in food selection, pp. 419-473. Waco, Tex.: Baylor Univ. Press. Wilcoxon, H. C., Dragoin, W. B., & Kral, D. A. (1971). Illness-induced aversions in rat and quail: Relative salience of visual and gustatory cues. Science, 171, 826-828.