Acquisition of representation-mediated conditioned food aversions

Food aversions were established in rats by administering lithium chloride (LiCl) immediately after the presentation of an exteroceptive conditioned stimulus (CS) which previously had been paired with a food substance. In Experiment 1, rats which received first tone-food and then tone-LiCl pairings showed less food consumption in subsequent testing than rats which received only tone-food or tone-LiCl pairings. Experiments 2 and 3 demonstrated the stimulus specificity of aversions established in this manner. Rats which first received pairings of light and tone CSs with two different food substances and then received pairings of one of those CSs with LiCl showed greater aversion to the food previously associated with the LiCl-paired CS than to the other food substance. Experiment 3 also showed that specific aversions were not acquired if rats received CS-shock rather than CS-LiCl pairings. These results suggest that CS-evoked representations of events can substitute for those events themselves in the formation of new associations.     

Postinjection suppression of drinking is modified by the presence of conditioned contextual cues: implications for both anticipatory and posttreatment nausea in humans

In three experiments, we set out to determine whether the response of rats to an injection of LiCl would be modified by the presence of an environmental context that had previously been paired with LiCl. Experiment 1 confirmed that one feature of the malaise produced by LiCl is a reduced tendency to consume an otherwise palatable flavor. Experiment 2 showed that the size of this response was enhanced if it was measured in the presence of a conditioned context. In Experiment 3, we investigated the possibility that the postinjection response could be modified by an overshadowing treatment given during the conditioning phase. The significance of these findings for the understanding of chemotherapy-induced nausea in the clinical population is discussed.     

Representation-mediated extinction of conditioned flavor aversions

Conditioned flavor aversions were extinguished by presenting without consequence auditory stimuli that had been previously paired with the aversive flavor. In Experiment 1, rats that received tone-sucrose pairings, then sucrose-lithium chloride (LiCl) pairings, and finally repeated tone-alone presentations showed greater sucrose consumption in subsequent testing than rats that received similar sucrose-LiCl pairings and tone-alone presentations but no initial tone-sucrose pairings. Experiment 2 demonstrated the stimulus specificity of the mediated extinction observed in Experiment 1. In Experiment 3, rats that received first-order light-food and second-order tone-light pairings prior to sucrose-LiCl pairings did not show greater subsequent sucrose consumption when extinction of the second-order tone intervened. These results suggest that conditioned stimulus (CS)-evoked representations of events can substitute for those events themselves in the extinction of previously established associations.     

Flavor preexposures in a conditioned taste aversion situation: a dissociation of behavioral and endocrine effects in rats

A series of experiments examined the effects of flavor preexposures on pituitary-adrenal/behavior relations in a conditioned taste aversion paradigm. It was found that reexposure to a novel milk solution paired earlier with lithium chloride (LiCl) elicited conditioned activation of the pituitary-adrenal system (Experiment 1). The unconditioned response to LiCl (measured by changes in plasma levels of corticosterone) did not vary as a function of prior (2 and 5 vs. 10) exposures to the milk solution (Experiment 2). Increased familiarity with the substance (resulting from 10 prior exposures) rendered the conditioning of a taste aversion to this substance less effective. Further, reexposure to this familiar substance after its pairing with LiCl was not accompanied by the characteristic conditioned pituitary-adrenal activation (Experiment 3). By titrating the number of conditioned stimulus (CS) preexposures (Experiment 4) it was found that within the range of preexposures manipulated (5-10), subjects exhibited (a) a coupling of behavioral and pituitary-adrenocortical responses when the conditioned taste aversion to the milk solution was paralleled by elevated plasma corticosterone (5-6 preexposures), (b) a coupling of these two response systems when flavor consumption was accompanied by suppressed plasma titers of corticoids (9-10 preexposures), or (c) a dissociation of the two system when the conditioned taste aversion was not accompanied by conditioned adrenocortical activity (7-8 preexposures). These data are discussed in terms of a dissociation in the effects of CS preexposures on conditioned adrenocortical and behavioral response systems.     

The influence of context and UCS intensity on the UCS preexposure effect in a flavor aversion paradigm

Three studies were conducted to evaluate the influence of environmental context and UCS preexposure intensity on the acquisition of a flavor aversion. In the first study, rats were exposed to two UCS-alone presentations at one of three dose levels of LiCl. The rats were given the two UCS preexposures in one of two contexts (familiar or novel). Following the UCS-alone treatment, all of the subjects received two pairings of sucrose and LiCl (1.25 meq) in the familiar context. Animals receiving UCS preexposures in the same context as used during conditioning consumed significantly more sucrose than did saline control animals. In contrast, the influence of prior UCS preexposure was not evident when UCS preexposure was experienced in a context different from that experienced during conditioning. In Experiment 2, all animal received UCS preexposure and conditioning in the novel room. Animals received either two or four preexposures at 0, 1.25, or 3.75 meq dose of LiCl. Two UCS preexposures at 3.75 meq dose produced a stronger UCS preexposure effect than did the 1.25 meq dose. Animals in Experiment 3 received two exposures to either 0-, 1.25-, or 3.75-meq LiCl in one of two contexts, followed by conditioning with the 1.25-meq LiCl dose in the same context as preexposure. Greater UCS interference occurred in animals preexposed to LiCl in the novel rather than familiar environment, with no specific dose effects in either context. These observations are discussed in terms of context blocking and generalization decrement models of the UCS preexposure effect.     

An extended comparator hypothesis account of superconditioning

Three conditioned taste aversion experiments with rats investigated superconditioning. In each experiment, alternate exposures of 2 flavor compounds with a common element (i.e., AB/AS) were administered to establish an inhibitory relationship between the 2 unique elements, B and S, and prior to testing, S was paired with lithium chloride (LiCl). In Experiment 1, pairings of a neutral cue (X) with S in compound with B after the AB/AS exposures resulted in superconditioning between X and S. Extinction of the common element (A) just before the S-LiCl pairing attenuated both the inhibitory relationship between B and S (Experiment 2) and superconditioning between X and S (Experiment 3). These observations suggest that superconditioning consists of enhanced performance rather than enhanced associative acquisition.     

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.     

Learned preference for a hedonically negative flavor is observed after pairings with positive post-ingestion consequences rather than with a palatable flavor

In two experiments, thirsty rats consumed a compound of sucrose and a non-preferred flavor. In Experiment 1, a conditioned preference was observed in the experimental group when animals were tested both thirsty and hungry, but not when they were tested just thirsty. Animals in the control group, which experienced the flavor and the sucrose unpaired, never showed a preference. Experiment 2 replicated the absence of a preference in the experimental group when rats were tested thirsty, but provided evidence that a flavor-taste association had been formed during training. After conditioning, sucrose was paired with LiCl in group Dev whereas it was unpaired in group NonDev. The sucrose devaluation produced a decrease in CS preference in group Dev, and an increment in group NonDev. Taken together, these results show that preference for a non-preferred flavor can be readily observed after pairings with the positive consequences of the US (calories or absence of an expected illness) rather than with a palatable flavor.     

Potentiation of odor by taste in rats: tests of some nonassociative factors

The contribution of nonassociative neophobia and sensitization to the potentiation of odor by taste in rats was tested in three experiments. In Experiment 1, neophobia for almond odor (O), saccharin taste (T), and odor-taste compound (OT) cues was tested before and after noncontingent lithium chloride poisoning and compared with conditioned aversions produced by OT-LiCl temporal pairing. The OT compound potentiated unconditioned neophobia, but there was no evidence of poison-enhanced neophobia, disinhibition of neophobia, or sensitization by noncontingent LiCl; temporal pairing produced aversions for the compound and its elements. In Experiment 2, generalization to a novel odor was tested after O-LiCl or compound OT-LiCl pairing. The potentiated odor aversion did not generalize to the novel odor; it was specific to the odor paired with taste and LiCl. In Experiment 3, potentiation of the odor component by a discriminant or nondiscriminant taste component was tested. Potentiation was evident only when a novel discriminant taste was in compound with odor prior to LiCl poisoning. These studies support an associative "indexing" hypothesis of the potentiation effect in rats.     

The effects of satiation and reinforcer develuation on signal-centered behavior in the rat

Two experiments are described which investigate the effects of satiation and reinforcer devaluation on signal-centered behavior in rats. In Experiment 1 lever contacts were established in hungry rats by pairing retractable lever presentations (CS) with response-independent food (UCS). Subsequently, food satiating these subjects significantly reduced the level of CS contact during an extinction test and, in particular, suppressed CS-directed licking and pawing. In Experiment 2 lever contacts which were established by lever-food pairings were suppressed when the food reinforcer was paired with lithium chloride (LiCl) induced illness. In particular, CS-directed licking, sniffing, and orienting were significantly suppressed by these food-LiCl pairings. These results suggest that signal-centered behavior (i) is not simply a manifestation of “conditioned hunger,” (ii) is determined to some extent by the animal's current need state, and (iii) is influenced by the status of specific reinforcer representations.     

Contextual control of negative transfer produced by prior CS-US pairings

When a conditioned stimulus (CS) is repeatedly paired with a weak unconditioned stimulus (US) prior to being paired with a stronger US in a second conditioning phase, interference, or negative transfer, is often observed during Phase 2. Two conditioned suppression experiments with rat subjects examined the effect of a context switch between phases in this “Hall-Pearce negative transfer paradigm.” In Experiment 1, negative transfer was obtained when the context remained the same for both phases, but there was no evidence of negative transfer when the context was switched between phases. Experiment 2 was designed to control for familiarity with the Phase 2 context, and showed that a context switch between phases again attenuated negative transfer. The effect of context on negative transfer was also similar to its effect on latent inhibition produced under comparable conditions. The results are not consistent with a model proposed by J. M. Pearce and G. Hall (Psychological Review, 87, 532–555, 1980), which ascribes no major role to the context in this situation, but are consistent with A. R. Wagner's (In S. H. Hulse, H. Fowler, & W. K. Honig, Eds., Cognitive Processes in Animal Behavior, pp. 177–209. Hillsdale NJ: Erlbaum, 1978) short-term memory model of conditioning, or with the view that contexts may signal specific CS-US relations. The results extend previous research on other interference paradigms, like latent inhibition and extinction, where context may play a similar role.     

Contextual control of fluid consumption: The effects of context extinction

Rats were trained on a conditional discrimination task in which saccharin was paired with LiCl in one context but paired with saline in another context. Rats drank less saccharin in the danger context than in the safe context, and consumption in the home cage was intermediate to consumption in the two training contexts. Rats also avoided the danger context on a choice test. After discrimination training, rats were given extinction trials with the danger context alone (Experiment 1 and 2) or with the danger context + water (Experiment 2). Extinction trials with the context + water abolished contextual control over saccharin consumption but not the avoidance of the danger context on the choice test. Extinction trials with the context alone abolished avoidance of the danger context but not contextual control over saccharin consumption. These data suggest that occasion setting, not simple context conditioning, is the mechanism by which contextual cues modulate fluid consumption.     

Examination of factors which might disrupt a learned association between pentobarbital and LiCl

Injections of a sedative dose of pentobarbital (Pent) were followed 30 min later by injections of a toxic dose of lithium chloride (LiCl). As a result of these Pent →LiCl pairings, injections of Pent after consumption of saccharin solution failed to produce the usual saccharin aversion. This loss of the capacity of Pent to produce a flavor aversion is called Avfail. Experiment 1 showed that the Avfail effect was obtained with saccharin even though the rats consumed a novel vinegar solution prior to the Pent→LiCl pairings in Phase 1. This was surprising since the novel flavor was associated with the LiCl and ought to have overshadowed the association of Pent with LiCl. Experiment 2 showed that one set of Pent→LiCl pairings can produce two Avfail effects in sequence: the first with a novel flavor and the second with a flavor previously paired with LiCl sickness. It also showed that insertion of Pent injections and handling cues between the Pent→LiCl and the Flavor→Pent phases did not reduce the magnitude of Avfail. Experiment 3 showed that the Avfail effect was not disrupted by the insertion of 54 saline injections between the Pent→LiCl and Flavor→Pent pairings, nor by interposing 26 saline injections between each pair of Flavor→Pent trials. This seemed to exclude an important role for injection cues. Experiment 3 also showed that 4 exposures to Pent and 50 exposures to saline between the Pent→LiCl trials and the Flavor→Pent trials and 26 exposures to saline injections between each pair of Flavor→Pent trials did not reduce the magnitude of Avfail. The same exposure to Pent and saline injections did reduce the magnitude of the saccharin aversion shown by the LiCl→Pent group. These data are viewed as consistent with Lett's (Drug-drug associations: Evidence for the conditioning of a compensatory response. Paper presented at a meeting of the Eastern Psychological Association, New York, 1981) suggestion that Avfail represents a learned antisickness response.     

Within-compound associations of taste and temperature

In two experiments, rats were given exposures to two solutions of different tastes (sucrose or sodium chloride) at two different temperatures (warm or cold). In Experiment 1, the rats were then given either one of the tastes at room temperature followed by LiCl injections, or distilled water at one of the temperatures followed by LiCl injections. Rats poisoned after drinking a taste were then given a choice between distilled water at the two temperatures, while those poisoned after drinking distilled water at a temperature were given a choice between the two flavors at room temperature. Rats drank less of the solution that contained the stimulus previously paired with the poisoned cue, demonstrating within-compound associations of tastes and temperatures. Experiment 2 found that tastes were better conditioned in a taste aversion procedure when the taste-temperature compound was the same during conditioning as during preexposure. This result is interpreted as evidence against a view of within-compound learning that treats the compound as a unitary stimulus.     

Extensive extinction in multiple contexts eliminates the renewal of conditioned fear in rats

Two studies examined whether nonreinforcement of a stimulus in multiple contexts, instead of a single context, would decrease renewal of conditioned fear in rats (as assessed by conditioned suppression of lever pressing). In Experiment 1, renewal was measured after 36 nonreinforced CS trials delivered during six extinction sessions in a single context or two extinction sessions in each of three different contexts. The number of extinction contexts did not have an effect on renewal. In Experiment 2, groups received either 36 or 144 nonreinforced CS trials during six or twenty-four extinction sessions in a single context or three different contexts. Again, renewal was not influenced by the number of extinction contexts when only 36 trials were given. However, when 144 trials were used, renewal was completely eliminated when extinction was divided between 3 contexts, but was not weakened when the sessions took place in a single context. The results suggest that the use of multiple treatment settings in exposure-based therapies is only likely to reduce relapse if a sufficient number of sessions are provided in each of the treatment settings.     

Conditioned taste aversion is enhanced when the unconditioned stimulus is presented in a different context

Using a conditioned taste aversion procedure with rats as the subjects, two experiments examined the effect of presenting a conditioned stimulus (CS saccharin solution) in one context followed by an unconditioned stimulus (US LiCl) in a different context. Experiment 1 showed that animals which received the above-mentioned procedure (Group D) showed a more marked conditioned aversion to the CS than animals which were given both the CS and the US in the same context (Group S). Experiment 2 found that in both Group D and Group S, aversion to the CS increased when the subjects were exposed to the conditioned context after the conditioning. These findings supported the argument that the strength of the CS-US association acquired during conditioning is compared with that of the context-US to determine the magnitude of aversion revealed to the CS.     

Conditioned Inhibition Produced by Extinction of a Conditioned Stimulus

Four experiments used a conditioned taste aversion procedure to examine the potential for CS-alone extinction treatment to produce a conditioned stimulus that possesses inhibitory properties. In Experiment 1, saccharin was paired with LiCl, and then saccharin was presented alone for several trials to produce extensive behavioral extinction. Animals receiving this treatment were retarded in reacquiring conditioned responding to saccharin relative to control subjects receiving conditioning to the flavor for the first time. In Experiment 2, the extinguished saccharin stimulus was shown to decrease conditioned responding to a known excitor when the two stimuli were presented in compound as a summation test. Experiments 3A and 3B replicated the findings of Experiments 1 and 2 while providing evidence that the effects were not due to the differential effects of neophobia during testing. These three experiments revealed that an extinguished conditioned excitor passes retardation and summation tests for conditioned inhibition. Experiment 4 found that extinction of a known excitor was slowed when the excitor was extinguished in compound with a previously extinguished conditioned stimulus. That is, an extinguished CS provided protection from extinction to another CS, a finding also consistent with the view that extinction produces conditioned inhibition.     

Context specificity of latent inhibition in taste aversion learning

In three experiments rats were given injections of LiCl after consuming distinctively flavoured water. The rats developed an aversion to the flavour and in all experiments the magnitude of the aversion was found to be reduced in subjects that had received pre-exposure to the flavour without aversive consequences. Experiment 1 demonstrated this pre-exposure effect to be a case of latent inhibition. The remaining experiments investigated the effects of pre-exposing the flavour in a context different from that used for conditioning. It was found (Experiment 2) diat latent inhibition transferred perfectly when the context change consisted of a move from one home cage to another. Context specificity of latent inhibition was found (Experiment 3) only when the subjects were given daily sessions in die experimental contexts, these being cages different from the home cage.     

Flavor preferences produced by backward pairing with wheel running

In 3 experiments rats given 8 sessions of preexposure to wheel running acquired a preference for a flavor that was given immediately after each of 4 subsequent sessions of wheel running. Such flavor preference was less likely when rats were given the same conditioning procedure but without preexposure to wheels (Experiment 1) or when access to flavor was delayed by 30 min following a wheel session (Experiment 2). When rats were given a flavor before each wheel session, the resulting conditioned aversion was greater in rats that had no prior exposure to wheel running (Experiment 3). These results show that whether an aversion or preference for a flavor is produced by wheel running depends on an interaction between prior wheel experience and the sequence of events.     

Differential Acquisition of Aversion by Two Distinctive Contexts Paired with Lithium-Induced Illness

In three experiments using rats as subjects, we investigated the role of the hedonic properties of the CS in context aversion conditioning. In Experiment 1, rats were allowed to drink water in two different contexts, L-S (Light room and Small cage) and D-B (Dark room and Big cage). Rats' consumption of water was higher in the D-B than in the L-S context. This result was taken as evidence for the L-S context eliciting a state of uneasiness that interferes with drinking plain water. In Experiments 2 and 3, rats were injected with lithium after placement in the L-S or the D-B context. In a blocking test (Symonds & Hall, 1997), the L-S context showed conditioning since it blocked the acquisition of aversion by a novel taste, quinine (Experiment 2) or salt (Experiment 3). By contrast, the D-B context failed to show conditioning, that is, no blocking was observed with salt or quinine. These results suggest that the hedonic properties of the context used as the CS may affect its acquisition of associative strength when paired with an internal aversive stimulus.