The Elusiveness of Gustatory Potentiation of an Environmental Aversion

Two experiments investigated conditions that influence whether or not the presence of a flavor cue potentiates acquisition of an environmental aversion. Experiments 1 and 2 exposed rats to either a salient sucrose flavor or nonsalient water with black box-illness pairings. Half of the rats in the sucrose and water treatment groups became ill after exposure to the black chamber in their home cage. The other half of the rats in the two treatment conditions became ill in the black box. The results of each study indicated that a strong environmental aversion was established when illness was associated with exposure to the black box. The aversiveness of the black chamber was indicated by both less time spent in the black side and reduced intake in the black chamber. The presence of sucrose during conditioning did produce a stronger black box aversion than did water. Reliable potentiation of the environmental aversion, however, was seen only when the illness experience occurred in the black chamber but not when illness occurred in the home cage. A weaker aversion to the black chamber was also found in the water groups when illness occurred shortly after experience with the black box than when illness immediately followed exposure to the black chamber.

     

Nonconsummatory and consummatory behavioral CRs elicited by lithium- and amphetamine-paired flavors

Various behavioral CRs elicited by saccharin solution previously paired with either lithium or amphetamine were measured in a series of four experiments. With one conditioning trial, lithium (Experiment 1), but not amphetamine (Experiment 2), produced nonconsummatory behavioral evidence of conditioning in the form of chin-rub CRs; both drugs, however, produced strong flavor aversions. With 3 conditioning trials, lithium- and amphetamine-paired flavors elicited a pattern of agitated activity, characterized by increased general activity, rearing duration, and body temperature, when the flavor was forcibly presented through an intraoral cannula (Experiment 3). When the flavor was presented in a single-bottle test (Experiment 4), 3 conditioning trials produced a similar pattern of agitated activity characterized by increased general activity, rearing (duration and frequency), stretching (duration and frequency), and limb flicking. Although both drugs supported the pattern of increased agitation-related CRs, only the lithium-paired flavors elicited chin-rub CRs (Experiments 1, 3, and 4). The difference between the drug conditions was not the result of a greater saccharin aversion in the lithium-conditioned group than in the amphetamine-conditioned group (Experiment 4). The results are related to findings that suggest that flavor aversions are mediated by a shift in the hedonic properties of the drug-paired flavors.     

Reinforcer devaluation in palatability-based learned flavor preferences

Rats exposed to simultaneous compounds of 1 neutral flavor with dilute (2%) sucrose and a 2nd flavor with dilute (2%) maltodextrin subsequently consumed both flavors in preference to a 3rd flavor that was never paired with a palatable taste. Brief training exposure under ad lib food and water minimized the post-ingestive effects of nutrients, emphasizing the contribution of palatability to these preferences. Devaluation of sucrose or maltodextrin by pairing with illness (Experiment 1) or sensory-specific satiety (Experiment 2) selectively reduced the preference for the flavor previously paired with the devalued reinforcer. Such reinforcer-specific devaluation effects suggest that palatability-based learned flavor preferences are under-pinned by a Pavlovian process whereby the cue flavor is associated with the taste of the concurrently consumed palatable reinforcer.     

Conditioned and unconditioned caloric compensation: Evidence for self-regulation of food intake in young children

The purpose of these two experiments was to determine (a) whether young children can be responsive to caloric density cues in regulating their food intake, (b) whether such cues can be associatively conditioned to organoleptic cues in foods, and (c) to obtain evidence regarding which of the many cues available are involved as conditioned stimuli. In Experiment 1 participants were eighteen 3- to 5-year-old children, who were seen for a series of pairs of conditioning trials, followed by extinction test trials. Each trial consisted of a two-part snack: approximately 100 ml of a pudding preload (chocolate or vanilla; high or low caloric density) followed after a delay by ad-lib consumption of snack foods (cookies and crackers). In extinction trials, flavors previously paired with high- or low-caloric density preloads during conditioning were presented in isocaloric intermediate density preloads. Results indicated that 14 of 18 children showed unconditioned caloric compensation on the first pair of conditioning trials; 16 of 18 children showed compensation following the second pair of trials, and 12 of these 16 subjects continued to show this consumption pattern during extinction. Consumption was significantly greater following the low calorie paired flavor than following the high calorie paired flavor during extinction. Experiment 2 (N = 10) replicated these findings, and uncorrelating preload and snack food flavors indicated that flavor cues in the preloads can serve as conditioned stimuli. Children showed both initial responsiveness to caloric density and evidence for associative conditioning of food cues to the physiological consequences of eating. These results provide initial evidence for a mechanism allowing the child to learn to anticipate the caloric consequences of familiar foods and regulate food intake accordingly.     

Second-order conditioning during a compound extinction treatment

Two conditioned taste aversion experiments with rats were conducted to establish if a target taste that had received a prior pairing with illness could be subject to second-order conditioning during extinction treatment in compound with a flavor that also received prior conditioning. In these experiments, the occurrence of second-order conditioning was indicated by protection from extinction of the aversion elicited by the target taste. This possibility, although intuitive, deserves attention because current associative models [e.g., 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 II: Current research and theory (pp. 64-99). New York: Appleton-Century-Crofts.] predict exactly the opposite outcome, namely, that compound extinction of two CSs should result in enhanced extinction.     

Selective association learning in the rat: Generality of response system

Three experiments with rats examined the possibility that the cue-consequence specificity effect is not mediated by the conditioning of selective associations, but instead reflects the selective behavioral expression of taste-illness and exteroceptive-shock conditioning. Experiment 1 showed that the selective aversion performance could be obtained despite the use of locomotor withdrawal from the CS as the index of conditioning. Experiment 2 compared the response profiles of animals conditioned with footshock or illness to presentation of a saccharin or noise CS. During the test with the noise CS, lithium-conditioned subjects did not differ from control rats on any of several behavioral categories, but shock-conditioned rats showed high levels of freezing in response to the noise cue. During the saccharin test, lithium-treated rats engaged in behaviors such as chin wiping, head shaking, and gaping; these behaviors were rarely or never seen in shock-conditioned rats or controls, whose behavioral profiles during the saccharin test were almost identical. Experiment 3, using a blocking design, found that a noise-lithium pairing did not attenuate subsequent conditioning of a saline-lithium association, nor did a saccharin-shock pairing interfere with conditioning of a noise-shock association. These results confirm that the cue-consequence specificity effect is mediated by the selective associability of taste with illness and of exteroceptive cues with footshock.     

A comparison of two methods of assessing representation-mediated food aversions based on shock or illness

In experiments that measured food consumption, Holland (1981; Learning and Motivation, 12, 1-18) found that food aversions were formed when an exteroceptive associate of food was paired with illness, but not when such an associate was paired with shock. By contrast, measuring the ability of food to reinforce instrumental responding, Ward-Robinson and Hall (1999; Quarterly Journal of Experimental Psychology, 52B, 335-350) found that pairing an associatively activated representation of food with shock readily established an aversion to that food. Two experiments considered the origins of these apparently discrepant results. The results did not support either the possibility that instrumental reinforcement power is a more sensitive measure of aversion learning than consumption, or the hypothesis that illness particularly devalues properties of food representations that determine consumption (such as palatability) whereas shock devalues more general properties critical to reinforcement. The results suggested instead that whereas the effects of pairings of a food associate with illness are mediated by changes in the value of the food itself, the effects of pairings with shock are mediated by the conditioning of fear or other competing responses to the site of food delivery, and not by modification of the value of food itself.     

The establishment of flavor-flavor associations using a sensory preconditioning training procedure

In Experiment 1, rats drank two distinct flavors in sequence during preconditioning; during training, the second of these flavors was paired with a toxin. During testing, there was an aversion to the flavor not directly paired with the toxin. In Experiment 2, the time interval between the two flavors (0, 3, 9, and 27 sec) in the preconditioning phase was varied; learning occurred only if the flavors were separated by 9 sec or less. Experiment 3, using a 60-sec interstimulus interval also did not reveal learning. These results reveal that the temporal gradient for flavor-flavor associative learning is similar to conventional audio-visual sensory preconditioning delay gradients and different from those obtained in flavor-toxicosis experiments. The results are discussed in terms of their critical implication for Revusky's concurrent interference theory of associative learning.     

Within-compound associations in a variety of compound conditioning procedures

Three experiments used a flavor-aversion preparation to demonstrate the occurrence of within-compound associations in various conditioning procedures. In Experiment 1 rats first received two separate two-flavor compounds, each followed by a mild US. They then received one element from one compound paired with a strong US and one element from the other compound nonreinforced. A subsequent choice test of the other two flavors from the compounds revealed that the consumption of each test flavor reflected the conditioning history of the element with which it had been paired. Rats drank less of the flavor whose associate had been paired with the strong US than of the flavor whose associate had been nonreinforced. In Experiment 2 within-compound associations were observed using a similar design in a blocking procedure in which one element from each of the two compounds was conditioned previously. Experiment 3 identified within-compound associations in a procedure where reinforced single element presentations were intermixed with nonreinforced compound presentations, as in a conditioned inhibition paradigm. These results suggest that within-compound associations occur in several important conditioning procedures which use multiple CS presentations.     

Age-dependent facilitation of taste-footshock conditioning by prior exposure to the training context

Among adult rats, gustatory stimuli are easily associated with illness, but not with external unconditioned stimuli such as footshock. Recent evidence indicates, however, that this cue-to-consequence specificity may vary ontongenetically. The present studies examined the acquisition of an aversion to a taste paired with footshock in 5- and 15-day-old rats. Consistent with previous reports, 5-day-old rats avoided the taste that preceded footshock, while 15-day-old subjects did not express an aversion to the taste paired with footshock. Exposure to the training context for either 1 or 5 h prior to conditioning disrupted taste-footshock conditioning in the 5-day-old subjects. For the 15-day-old subjects, 1 h of pre-conditioning exposure to the training context had no effect on conditioning, whereas a longer duration of preexposure promoted conditioning to the taste cue. The results suggest ontogenetic differences in stimulus selection.     

Unconditioned stimulus devaluation effects in nutrient-conditioned flavor preferences

Experiments with different temporal relations between the conditioned stimulus (CS) and the unconditioned stimulus (US) in conditioning assessed whether US devaluation effects can be obtained after nutrient-conditioned flavor preference learning. One flavor (CScarb) was paired with a carbohydrate, Polycose; a 2nd flavor (CSprot) was paired with a protein, casein; and a 3rd flavor (CS-) was presented by itself. Following conditioning, one of the nutrients was devalued through pairings with lithium chloride in the absence of the CS flavors. In a subsequent 2-bottle test, rats preferred CScarb over CSprot; however, this preference was smaller when the carbohydrate was devalued than when the protein was devalued. Results suggest that CS flavors are able to form associations with the sensory features of nutrient USs under a wide variety of circumstances.     

The role of cue additivity in salience in taste aversion conditioning

In toxiphobia conditioning certain cues are more easily associated with malaise (i.e., more salient) than others. The present experiments show that cue additivity can account for previously found differences in salience of certain fluids. The relative salience of saccharin, saline and casein hydrolysate was tested in normal rats and in animals rendered anosmic by treatment of their nasal passages with zinc sulphate. The normally more salient casein was reduced in salience to the same level as saccharin and saline in the anosmic animals, while anosmia did not affect the relative salience of saccharin and saline. A second study tested the cue properties of vanilla, a fluid of very low salience. Anosmic animals could not show a conditioned aversion to vanilla. Normal animals readily learned the aversion but could not show it following a later anosmia treatment. Anosmia did not disrupt a saccharin aversion previously conditioned in normal animals. The data show that some of the “tastes” used in toxiphobia conditioning have olfactory components, and some are purely olfactory. Further, olfactory cues can summate with taste cues to form a more salient stimulus.     

Conditioned enhancement of human's liking for flavor by pairing with sweetness

This paper reports a procedure, like classical conditioning, that produces enhancement of liking for flavors by humans. The procedure is “pairing” of a relatively neutral flavor with sugar (a hedonically positive taste). Specifically, subjects drank 24 small samples of flavor A sweetened and 24 small samples of flavor B unsweetened. They were then tested for their liking for flavors A and B, both sweetened and unsweetened. In three different studies, varying in a number of aspects of stimulus presentations and context, a relative enhancement in liking for flavor A appeared both on the day of exposure and 1 week later. An absolute enhancement in liking of flavor B (a “mere exposure” effect) also occurred in two of the three experiments.     

Developmental flavor experience affects utilization of odor, not taste in toxiphobic conditioning

Feeding experiences were varied in developing rats and the effects upon flavor neophobia and lithium chloride-induced flavor aversions were observed. In Experiment 1, nursing experience of neonate rats was reduced by artificial feeding via intragastric cannula; the rats then were tested with apple juice paired with lithium chloride injection at weaning or maturity. Conditioned aversions were not affected, but neophobia to novel apple juice was attenuated in artificially-reared rats tested at maturity. In Experiment 2, rats received enriched feeding experience after weaning, which consisted of (a) obtaining many complex flavors, a few of which were paired with poisoning, effortlessly in the home cage, or (b) foraging for various foods on an elevated maze. No dramatic effects on neophobia or conditioned taste aversion for saccharin water were apparent. In Experiment 3, rats were given experience after weaning with vanilla-scented water either paired or unpaired with quinine water, and then tested with the odor of almond or that odor compounded with saccharin water for neophobia and lithium-induced aversions. Flavor-experienced rats exhibited more pronounced odor conditioning and more resistance to extinction of the odor aversion after both simple and compound conditioning. In contrast, saccharin taste aversions were relatively unchanged. Apparently, enriched feeding and drinking experience facilitates the utilization of odor more than taste cues.     

Drug-preexposure effects in flavor-aversion learning: associative interference by conditioned environmental stimuli

Previous research has documented that exposure to a drug reduces the ability of the drug to support subsequent flavor-aversion learning. The four experiments reported here examined the hypothesis that this drug-preexposure effect is due to associative interference from environmental stimuli associated with the drug effects during preexposure. When distinctive environmental stimuli (confinement in a black compartment) were present during drug preexposure, these stimuli significantly disrupted subsequent flavor-aversion learning. Furthermore, flavor conditioning was not significantly disrupted when drug preexposure occurred in the absence of salient environmental stimuli or when the previously conditioned environmental stimuli were extinguished prior to flavor conditioning. It is significant, and in contrast to other published research, that flavor conditioning was not disrupted when the distinctive cues paired with the drug during preexposure were absent at the time of the flavor-drug pairing. These results are thus consistent with results from conventional studies of stimulus blocking and suggest that associative processes can play a major role in the drug-preexposure effect.     

Retrospective Revaluation or Mediated Conditioning? The Effect of Different Reinforcers

It is becoming accepted that the associative strength of a cue can change in its absence. However, the rules that govern the association of the representations of absent cues are in dispute. There is evidence to support both the idea that the representation of a cue is associated in the same fashion as the cue itself (e.g. Holland, 1990) and the contrary idea that the representation will be associated in the opposite manner to the cue itself (e.g. Dickinson & Burke, 1996). In three experiments an aversion to almond was formed by the pairing of the induction of nausea by lithium chloride injection with a context previously paired with almond. In addition in the third experiment an aversion was formed to almond when a flavoured solution previously paired with quinine was drunk in a context previously paired with almond. These results suggest that the rules governing the association of the representations of absent cues depend on the type of reinforcer.     

Salience and the effects of CS preexposure on aversion conditioning

Rats (n = 84) received preexposure to distilled water or to one of two differently salient flavors, 5.0% casein or 10.0% sucrose, casein being the more salient. Each preexposure group then received aversion conditioning to a 5.0% casein or a 10.0% sucrose CS. Aversion effects were reliably more enduring to casein than to sucrose. Relative to water-preexposed groups, preexposure to casein attenuated aversion effects to the casein CS reliably less than preexposure to sucrose attenuated aversion effects to the sucrose CS. During preexposure, neophobia was reliably greater to casein than to sucrose, suggesting that the demonstration of salience in taste aversion learning may be based on the inherent aversive properties of novelty.     

Perceptual learning in flavor aversion: evidence for learned changes in stimulus effectiveness

Rats were exposed to the compound flavors AX and BX, presented in alternation, and to CX on a separate block of trials. Generalization to BX after aversion conditioning with AX was less than to CX. An equivalent effect was found when the nature of the common element was changed after preexposure but not when the common element was omitted during preexposure, during conditioning and test, or both. Rats conditioned with X alone again showed less aversion to BX than to CX; similarly, rats conditioned with a novel flavor (Y) showed less aversion to BY than to CY. These effects support the proposal that intermixed preexposure to AX and BX enhances the perceptual effectiveness of their unique features, A and B.     

Long-delay taste aversion learning in an unpoisoned rat: Exposure to a poisoned rat as the unconditioned stimulus

M. J. Lavin, B. Freise, and S. Coombes (Behavioral and Neural Biology, 1980, 28, 15–33) have shown that if two rats consume a flavored solution and one is poisoned, the unpoisoned partner will also exhibit a flavor aversion during a later preference test. Experiments 1 and 2 showed that a sufficient condition for obtaining this aversion is that the poisoned partner be present with the unpoisoned rat after it has consumed the flavored solution. It is not necessary that the poisoned partner be present when the flavored solution is consumed or indeed have had any exposure to the flavored solution. Experiment 3 showed that the unpoisoned partner can exhibit a flavor aversion when there is a temporal gap of as long as 6 hr between consumption of the flavored solution and exposure to the poisoned rat.