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The effects of chronic lead exposure on taste-aversion conditioning in rats.

Recent reports have shown that lead contamination results in an increase in emotionality in humans (Baker, Feldman, White, & Harley, 1983; David, Clark, & Voeller, 1972) and animals (J. C. Flynn, E. R. Flynn, & Patton, 1979). For example, chronic lead exposure has been shown to exacerbate reactivity to primary (Nation, Baker, Fantasia, Ruscher, & Clark, 1987) and secondary (Nation, Clark, Bourgeois, & Rogers, 1982) aversive stimuli. Likewise, a recent study by Davis, Nation, and Mayleben (in press) demonstrated that lead-exposed animals experiencing partial reinforcement runway training prior to extinction took longer to extinguish the running response than did nontoxicant-exposed partial reinforcement animals. These results were interpreted as reflecting stronger conditioning of frustration-generated cues to the instrumental running response by the lead-exposed animals during partial reinforcement training. Thus, when extinction was begun the lead-exposed animals persisted longer than did their non-lead-exposed counterparts.

The logic employed by Davis et al. (in press) in accounting for their runway results may be extrapolated to the situation in which lead-exposed animals are subjected to conditioned taste aversion procedures. If lead exposure enhances reactivity to aversive stimuli (e.g., Nation et al., 1987; 1982), then it is predicted that lead-exposed animals will develop stronger taste aversions than non-lead-exposed animals because of a more intense reaction to the unconditioned stimulus (US). More directly, the heightened reactivity shown by the lead-exposed animals may become functionally equivalent to the use of a more intense US. As US intensity has been shown to be positively related to the strength of taste-aversion conditioning (Dragoin, 1971; Garcia, Kimeldorf, & Koelling, 1955; Nachman & Ashe, 1973; Revusky, 1968), animals receiving lead-exposure should develop stronger aversions. The present experiments sought to evaluate this prediction. In order to evaluate differential effects that might be associated with the specific type of US, illness was induced both by chemical (Experiment 1) and mechanical (Experiment 2) means.

Experiment 1

The strength of taste-aversion conditioning of a novel saccharin flavor in lead-exposed and non-lead-exposed animals was directly evaluated in Experiment 1. Lithium chloride (LiCI) was used to produce toxicosis.


Subjects and apparatus. Thirty-two male Holtzman rats served as subjects. The animals were 44 days old at the inception of the lead-exposure phase, and 150 days old at the time of conditioning. All subjects were individually caged in standard, suspended, wire-mesh cages (1 7.78 cm x 17.78 cm x 24.13 cm) in the animal vivarium. A 12/12 light/dark lighting cycle was in effect for the duration of the experiment.

Laboratory chow was available on a free-feeding basis for the duration of the experiment. All testing was conducted in the home cage and took place daily at 1300 hours, during the lights-on cycle.

Procedure. One half of the animals were selected to receive lead exposure for a 100-day exposure phase that preceded the experiment proper. Lead exposure was accomplished by mixing .92 grams of lead acetate per liter of water; this procedure yielded a solution having 500 ppm lead. This solution was available on an ad libitum basis. The remaining 16 animals were maintained on plain tap water during the exposure phase. Fluid consumption (grams) was recorded every 2 days during the exposure phase. Additionally, all animals were weighed every 4 days during the course of the experiment.

Five days prior to conditioning all subjects were placed on a fluid-deprivation regimen that allowed them free access to water for 15 min daily. In addition to habituating the subjects to the water-deprivation schedule, this 5-day period served to establish a fluid-consumption baseline for each subject.

At the completion of the baseline phase, two equal-sized subgroups (n = 8) of lead-exposed animals and two equal-sized subgroups (n = 8) of water-exposed were randomly formed. In turn, one lead-exposed subgroup (Group PB-Li) and one water-exposed subgroup (Group W-Li) were randomly selected to receive LiCI-induced toxicosis on conditioning. The remaining two groups, one lead-exposed (Group PB-S) and one water-exposed (Group W-S) received an injection of nontoxic saline on conditioning.

Conditioning involved the following procedures. First, each subject was allowed to consume saccharin (.15%, w/v) for 15 min. Following saccharin consumption each subject received a .12% body weight intraperitoneal (ip) injection. Subjects in Groups PB-Li and W-Li were injected with .15M LiCI, and subjects in Groups PB-S and W-S were injected with .09% normal saline.

The first of five, daily two-bottle preference tests (saccharin vs. water) was begun 24 hr following conditioning. Graduated, 50-ml centrifuge tubes fitted with spill-resistant sippers were used to dispense fluids during baseline, conditioning, and preference testing. In all cases fluid consumption was recorded to the nearest .50 ml.

Forty-eight hours after testing, the animals were rendered unconscious and then decapitated. Trunk blood was collected for each animal. The concentration of lead in blood was measured by atomic absorption spectrophotometry.


A repeated-measures of variance (ANOVA) of the consumption scores recorded by the lead-exposed and water-exposed animals during the exposure phase yielded significance only for the days factor, F(49, 1500) = 1.94, p < .01. Thus, it can be concluded that although both groups increased general fluid consumption during the exposure phase, they did not differ with regard to the amount of fluid that was consumed.

The lack of significant between-groups consumption differences during the baseline period, F(1, 30) = 1.35, p > .25, and on conditioning, F(3, 28) = 1.32, p > .25, also serve to establish group equivalence prior to the first two-bottle preference test. However, a comparison of fluid consumption on the final day of baseline with that of conditioning revealed the occurrence of a significant neophobic effect, F(1, 32) = 8.47, p < .01. Significantly less fluid was consumed on conditioning than on the last day of baseline.

The results of the five, daily two-bottle preference tests are shown as consumption ratios in Figure 1. These consumption ratios were formed by dividing saccharin intake by total fluid intake. A ratio of .50 thus reflects equal consumption of saccharin and water, whereas ratios lower than .50 reflect saccharin aversions. Ratios greater than .50 reflect a saccharin preference. A repeated measures ANOVA, incorporating exposure fluid (lead vs. water) and conditioning injection (saline vs. LiCI) as between-subjects factors and days as a within-subjects factor, was performed on these consumption ratios. The results of this analysis yielded significance for the conditioning injection, F(1l, 28) = 21.26, p < .001, and exposure fluid x conditioning injection x days, F(4, 112) = 4.13, p < .01 , effects. Of particular interest to the present project are the results of subsequent Newman-Keuls tests which indicated that the consumption ratios of Group PB-Li were significantly (p < .05) below those of Group W-Li on Preference Tests 1-3. Although this same differential was maintained on Preference Tests 4 and 5, these differences failed to achieve significance.

Analysis of trunk blood residue yielded significance, F(1, 28) = 9.65, p < .01, only for the lead-exposure factor. Greater concentrations of the metal were found in the blood of the lead-exposed animals (M 0.233ppm) than that of the non-lead-exposed animals (M = 0.029ppm).


Several points of interest emerge from a consideration of Figure 1. First, it is clear that, regardless of type of fluid exposure, those animals that received the saccharin-LiCI pairing developed strong saccharin aversions. As both groups of LiCI-injected animals failed to display a saccharin preference during the course of preference testing, it can be concluded that these aversions were rather long-lasting in nature. Clearly, preferences, not aversions, were shown by the two groups of saline-injected animals.

Second, the rather stable pattern of responding demonstrated by both groups of saline-injected animals during preference testing is worthy of note. The consistent preference for saccharin that existed across this 5-day session indicates that the neophobic response had effectively dissipated by the first preference test.

Finally, the differential aversions displayed by Groups PB-Li and W-Li deserve special note. That the aversion of Group PB-Li was significantly stronger than that of Group W-Li on the first 3 days of preference testing suggests that any added reactivity engendered by lead exposure was translated into measurable behavioral differences. The fact that this difference persisted for 3 days would lead one to speculate that this effect is not especially fragile in nature.

Experiment 2

The positive support provided for the lead-reactivity prediction notwithstanding, the results of Experiment 1 might be subject to a different interpretation. It is arguable that, for some unknown reason, joint exposure to lead and LiCI resulted in a chemical reaction that enhanced the toxic effect of the US. Although the details of such a chemical interaction might be interesting to ascertain, numerous studies previously have established the fact that stronger USs produce stronger taste-aversions. If, however, a stronger taste-aversion can be established in lead-exposed animals when a non-drug US is employed, then the added emotionality interpretation would gain increased credence. Because of its successful use in previous studies of taste-aversion conditioning (e.g., Braun & McIntosh, 1973; Braveman, 1975; Davis, Best, Grover, Bailey, Freeman, & Mayleben, 1990; Green & Rachlin, 1973), rapid rotation was selected as the US in Experiment 2.


Subjects. Thirty-six male Holtzman rats served as subjects. The animals were 170 days old at the time of testing. All animals were individually caged with food available on a free-feeding basis for the duration of the experiment.

Apparatus. The conditioning apparatus consisted of a Lafayette (Model 13012) color mixer. The inside edge of a 10.00-cm (inside diameter) plastic jar was mounted 6.25 cm from the center of the 20.32-cm-diameter rotating aluminum disc. The variable speed control allowed the number of revolutions per minute to be set at 180. All preference testing took place in the home cage.

Procedure. One half of the animals were randomly selected to receive lead exposure for 100 days immediately preceding the experiment proper. Lead exposure was accomplished as in Experiment 1. The remaining animals received free access to plain tap water. Fluid consumption and weight data were gathered in the same manner as in Experiment 1.

Five days prior to conditioning all subjects were placed on a fluid-deprivation regimen that allowed them access to water for 15 min daily In addition to habituating the subjects to the water-deprivation schedule, this 5-day period served to establish a water-consumption baseline.

Two equal-sized subgroups (n = 9) of lead-exposed animals and two equal-sized subgroups (n = 9) of water-exposed animals were randomly formed at the end of baseline. In turn, one lead-exposed subgroup (Group PB-R) and one water-exposed subgroup (Group W-R) were randomly selected to receive rotation-induced taste-aversion conditioning. The remaining lead-exposed subgroup (Group PB-NR) and the remaining water-exposed subgroup (Group W-NR) served as nonrotation controls.

Conditioning was conducted 24 hr following the final baseline session. On the conditioning day each subject was allowed to consume saccharin (.15%, w/v) for 15 min. Following saccharin consumption, taste-aversion subjects in Groups PB-R and W-R each received a 1-min rotation period to induce illness. Subjects in the two nonrotation control groups (Groups PB-NR and W-NR) each received a 1-min placement in the apparatus.

The first of four, daily two-bottle preference tests (saccharin vs. water) was begun 24 hr following conditioning. During baseline, conditioning, and preference testing all fluids were dispensed and measured as in Experiment 1.


As in Experiment 1, an ANOVA performed on the consumption scores recorded during exposure yielded significance, F(49, 1700) = 2.11, p < .01, for the days factor. Thus, although intake increased across days, it did not differ between the lead- and water-exposed animals.

Analyses of the consumption data during baseline, F(1, 34) = 1.31, p > .25, and on conditioning, F(3, 32) = 1.28 , p > .25, failed to yield reliable differences between the lead- and water-exposed animals. Hence, these animals were deemed comparable, with regard to fluid consumption, prior to the start of preference testing. The occurrence of a significant neophobic effect was revealed via the consumption of significantly, F(1, 34) = 8.53, p < .01, less fluid on conditioning than on the last day of baseline.

Mean consumption ratios ( saccharin/saccharin+water) for the four preference tests are shown in Figure 2. A repeated measures ANOVA of these consumption ratios yielded significance for the days, F(3, 96) = 3.53, p < .05, type of conditioning injection, F(1, 32) = 6.92, p < .05, days x type of conditioning injection, F(3, 96) = 5.18, p < .01, and days x exposure fluid x type of conditioning injection, F(3, 96) = 3.92, p < .05, factors. Subsequent Newman-Keuls tests indicated that the consumption ratios of Groups W-R and PB-R were significantly below (p < .01) those of Groups PB-NR and W-NR on Preference Test 1. Additionally, the consumption ratios of Group PB-R were significantly (p < .05) below those of Group W-R on Preference Test 1. The consumption ratios of Group PB-R also fell significantly (p < .05) below those of all other groups on Preference Test 2.

As in Experiment 1, analysis of the trunk blood residue yielded significance, F(1, 32) = 10.18, p < .01, only for the lead-exposure factor. The blood of the lead-exposed animals (M = 0.219ppm) contained greater concentrations of the metal than that of the non-lead-exposed animals (M = 0.031 ppm).


As the consumption ratios of the nonrotated subjects (Groups PB-NR and W-NR) were consistently above .50, these subjects displayed saccharin preferences, not aversions. The significantly lower consumption ratios shown on Preference Test 1 by the rotated subjects (Groups PB-R and W-R) indicate that saccharin aversions had been established. Moreover, the finding that the consumption ratios of Group PB-R were significantly lower than those of Group W-R indicates that a stronger aversion was established by the lead-exposed animals. This finding is in accord with the results of Experiment 1. However, the rapid diminution of this between-group difference indicates that the rotation-induced effect is more transitory than its LiCI-induced counterpart.

General Discussion

The two experiments reported here demonstrate the development of stronger taste aversions in lead-exposed rats. In Experiment 1 taste aversions were conditioned via chemically induced (LiCI) toxicosis, and illness was induced in a non-chemical manner (rapid rotation) in Experiment 2. Thus, the enhanced aversions shown by the lead-exposed animals cannot be attributed to the chemical interaction of lead and the illness-inducing toxin. Had this chemical interaction been responsible for the present results, the lead-exposed animals in Experiment 2 would not have displayed stronger aversions.

The present results are supportive of the prediction that increased reactivity engendered by lead exposure would result in stronger conditioned taste aversions. Although the specific mechanism by which this process takes place was not tested by these experiments, the following account appears to be a likely candidate.

If one assumes that the heightened reactivity produced by lead exposure results in the creation of additional, albeit internal, stimuli that are potentially available to enter into conditioned associations, then a situation that is analogous to taste-mediated potentiation exists. In taste-mediated potentiation experiments a compound CS is followed by illness. Subsequent tests indicate that aversions to one element of the compound CS are potentiated, relative to that element conditioned by itself. For example, the aversion to an odor can be potentiated by presenting that odor in compound with a taste on the conditioning trial (e.g., Coburn, Garcia, Kiefer, & Rusiniak, 1984; Left, 1984; Palmerino, Rusiniak, & Garcia, 1980). Similarly, the presentation of two tastes as a compound CS can potentiate the aversion to one of the tastes (Bouton, Dunlap, & Swartzentruber, 1987; Davis, Best, & Grover, 1988). A within-compound theory of multiple associations has been employed to account for such potentiated aversions (e.g., Davis et al., 1988; Durlach & Rescorla, 1980). This account proposes that the establishment of additional associations between the elements of the compound CS and the US and associations linking the elements of the CS results in the display of a potentiated aversion.

Just as the elements of the compound CS used in taste-mediated potentiation experiments can enter into additional associations, we suggest that the additional stimuli that result from lead exposure in the present experiments also can enter into associations with the aversive US, as well as the taste CS. The influence of these additional associations was manifested in the form of stronger saccharin aversions by the lead-exposed animals of Experiments 1 and 2.

Whereas the linkage between lead exposure and enhanced taste aversion is robust and rather straight forward, one aspect of both experiments is problematic for the present interpretation. If lead exposure increases reactivity to aversive stimuli, then it might also be predicted that the lead-exposed animals would display a stronger neophobic response to the novel saccharin on the day of conditioning. However, differential neophobic responses between the water- and lead-exposed animals did not exist in either experiment. Although the failure to detect differences in neophobia does not invalidate the reactivity account, it is clear that additional research will be needed to (1) more clearly identify those stimuli that do result in enhanced reactivity, and (2) provide additional, independent indexes of the heightened reactivity.


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Author:Davis, Stephen F.; Freeman, Bobby L.; Nation, Jack R.
Publication:The Psychological Record
Date:Mar 22, 1993
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