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Acquisition of representation-mediated conditioned food aversions
LEARNING
AND
MOTIVATION
12, I-18 (1981)
Acquisition of Representation-Mediated Conditioned Food Aversions PETER C. HOLLAND University
of Pittsburgh
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-LiCI pairings showed less food consumption in subsequent testing than rats which received only tone-food or tone-LiCI 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 LiCI-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-UC1 pairings. These results suggest that CS-evoked representations of events can substitute for those events themselves in the formation of new associations.
Many recent theories presume the involvement of internal representations of the conditioned stimulus (CS) and the unconditioned stimulus (US) in Pavlovian conditioning. For instance, Konorski (1967) and Rescorla (1974) suggested that conditioned responding develops when the CS comes to activate a US representation which prior to conditioning could only be evoked by the US itself. The experiments reported here examined some of the properties of the US representations evoked by css. Considerable data support the claim that US representations are involved in the generation of conditioned responding. Rescorla and his colleagues for example (Holland & Rescorla, 1975; Rescorla, 1978) have performed a number of experiments in which the affective value of the US representation was modified after conditioning of a CS. Since conditioned This research was supported in part by Grant BNS 7903853 from the National Science Foundation. Thanks are due to Kathy Allen, who assisted in data collection in Experiment 3. Requests for reprints should be sent to Peter Holland, Department of Psychology, University of Pittsburgh, Pittsburgh. Pa. 15260. 0023-%90/81/010001-18$02.00/O Copyright @ 1981 by Academic Press. Inc. A11 rights of reproduction in any form resewed.
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C. HOLLAND
responding is presumably produced by activation of the US representation by the CS, modification of that representation should be reflected in subsequent responding to the CS. Responding to the CS was in fact observed to track postconditioned changes in US value in their experiments. Many theorists have assumed that in some respects activations of a US representation by either the US itself or by a CS are equivalent. For instance, Konorski (1967) attributed the frequently observed similarity of conditioned responses (CRs) and unconditioned responses (URs) to the fact that both responses are produced by activation of the same US representation. And Wagner and his colleagues (e.g., Terry, 1976; Wagner, 1978) found that various interference effects attributed to priming of a representation of the US into a short-term memory system occur whether that representation was primed directly by the US itself or was retrieved by a CS previously paired with that US. The experiments reported here examined the ability of a representation of an event retrieved from memory to substitute for that event itself in the formation of new associations involving that event. In Experiment I, an aversion to a food substance was produced by inducing illness immediately after the evocation of a representation of that food, in the absence of food itself. Experiments 2 and 3 examined the stimulus specificity of food aversions established in this manner. EXPERIMENT
1
In Experiment 1, a tone CS was repeatedly paired with food, presumably endowing that tone with the ability to evoke a representation of the food US. Then presentation of the tone alone was paired with the injection of an illness-inducing agent, lithium chloride. Finally, consumption of the food was tested. If the food representation evoked by the tone was sufficiently similar to the food US itself to enter into associations in a like manner, the tone-lithium chloride pairings might be anticipated to establish an aversion to that food, even though food itself was never paired with illness. Method Subjects. The subjects were 32 male Sprague-Dawley rats about 100 days old at the beginning of the experiment. They received unrestricted access to water but were deprived of food so as to maintain them at 80% of their ab lib weights. The rats were housed individually in stainless-steel cages measuring 17.8 x 25.4 x 17.8 cm. Apparatus. The experimental chambers consisted of eight identical chambers, 22.9 x 20.3 x 20.3 cm. Each chamber had a dimly illuminated, recessed food cup in the center of one end wall; these cups were fitted with photocells which activated circuitry in an adjoining room whenever a
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FOOD AVERSIONS
rat’s head was inserted about 6 mm or more into the food cup. A similar food cup projected 3.7 cm into the chamber from the center of the other end wall; this cup was not used in Experiment I. To the left of the recessed food cup was an inoperative standard rat lever. The floor of the chamber was composed of 0.48-cm stainless-steel rods spaced 1.9 cm apart. The two end walls were aluminum; the side walls and top were clear acrylic plastic. Each chamber was enclosed in a light- and soundresistant closet. A speaker and a 6-W houselight were mounted on the inside wall of each closet enclosure, about IO cm above and in front of the experimental chamber. Procedure. An outline of the procedures of Experiment I is given in Table 1. Rats were randomly assigned to four groups of eight rats each and Phase I, designed to endow a tone CS with the ability to evoke a representation of food in some rats, was begun. In each of the eight daily sessions of Phase 1, rats in Groups TT and TL received four reinforced presentations of a 10.5set 1400-Hz (75 db SPL) tone and four nonreinforced presentations of a IO-set flashing (2/set) houselight. Rats in Group LT received four reinforced presentations of the IO.5set flashing houselight and four nonreinforced presentations of the IO-set 1400-Hz tone during each of these sessions. Rats in Group BT received four IO-set houselight CSs and four IO-set tone CSs in each Phase I session; reinforcements were delivered 5 set before each tone presentation. (The first letter of the group designations indicates whether rats received Tonefood, Light-food, or Backward food-tone pairings in Phase I .) The reinforcing event used in Phase 1 was the delivery of two 45-mg wintergreenflavored sucrose pellets (P. J. Noyes Co.) during the last 0.5 set of reinforced CSs. Feeder operation produced an audible click. Thus, at the end of Phase 1, the tone would be expected to evoke a representation of the wintergreen food pellets in Groups TT and TL, but not in Groups LT or BT. Each Phase 1 session was 75 min long; no trials were presented during the first 15 min of any session. Intertrial intervals averaged 7.5 min and were distributed rectangularly with a range of 4.5-10.5 min. Light and TABLE 1 Procedures of Experiment
I
Phase I Group Group Group Group
TT TL LT BT
T+fd,L+4 T-+ fd, L -+ 4 T-+q&L-+fd fd +T. L+ 4
Phase 2 Food Food Food Food
pretest pretest pretest pretest
T T T T
---) LiCI. + 4. L --, LiCI, -+ LiCI,
L + L L
-+ I$ LiCl -+ 4 -+ 4
Food Food Food Food
test test test test
Note. T, tone; L, light; 4, no explicit stimulus; fd, food; LiCI, lithium chloride injection.
groups were placed in the experimental chambers for the usual 15min stimulus-free period. Then a single stimulus was presented, immediately after which the rats were removed from the experimental chambers. On Days I and 3 of Phase 2, rats in Group TT received a 10.5set tone CS terminating in feeder operation (as in Phase l), but pellets were not delivered. Each rat was injected with 0.3 M lithium chloride (LiCl), 0.5% body weight, as it was removed from its experimental chamber. Because rats were run in squads of eight, the actual tone-injection interval ranged from 30 set to 5 min in each group. After the injections, each rat was placed in a small holding cage until all rats in that group had received injections; they were then returned to their homecages. Rats in Groups LT and BT received similar treatment except (as in Phase 1) the tone CS was 10 set long and was not accompanied by feeder operation. Rats in Group TL received similar injection treatment but received a IO-set light stimulus (unaccompanied by feeder operation) rather than the tone preceding each injection. (The second letter of the group designation indicates whether Tone or Light was paired with LiCl injection in Phase 2.) On Days 2 and 4 of Phase 2, rats in Groups TT and BT received a IO-set light stimulus; immediately after the light presentation the rats were placed in the holding cage for 5 min and then returned to their homecages. Rats in Group LT received similar treatment except the light was 10.5 set long and accompanied by feeder operation (but not pellet delivery). Rats in Group TL received a 10.5-set presentation of the tone accompanied by feeder operation (but not pellet delivery) on each of these 2 days. Thus, only the rats in Group TT had a CS-evoked representation of the food pellet US paired with LiCl injection. Finally, on the next day, all rats received a consumption test identical to the pretest of consumption described above. The primary data in these experiments were the number of food pellets consumed in the homecages during the various food consumption tests. In addition, food cup entries were recorded in the experimental apparatus. Output of the photocell circuits was interrogated at I-set intervals during the CS presentations and during the 30-set periods prior to CS presentations. The number of interrogations on which a rat had its head in the food
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cup during an interval was divided by the total number of interrogations during that interval to generate the measure “percentage cup responding.” This measure was selected as an index of conditioning since previous experiments (e.g., Holland, 1977) indicated that both auditory and visual CSs evoke food cup entry (magazine) behavior to some extent. Results Cup responding during reinforced CSs increased steadily over the course of Phase 1. The left side of Table 2 shows percentage cup responding during pre-CS, tone CS, and light CS intervals over the last two sessions. Every rat showed greater cup responding during the reinforced CS than during either the pre-CS period or the nonreinforced CS. Tone responding was reliably less in Group LT than in the other three groups (Mann-Whitney U’s c 8) which did not differ among themselves. The superiority of Groups TT and TL to Group LT indicated that the tone was conditioned in the former two groups. The superiority of Group BT, however, is likely to be more attributable to the rats’ consuming food pellets during CS presentations than to backward conditioning (see below). The percentage of cup responding during the light stimulus was greater in Group LT than in any of the other groups (U’s c 1 I), which did not differ from each other. The lower level of cup responding during the reinforced light CS than during the reinforced tone CSs probably reflects the occurrence of conditioned behavior to the localized light source (rearing) which is incompatible with the measured cup response (cf. Holland, 1977) rather than any substantial difference in the amount of conditioning. Pre-CS responding did not differ among the groups. Median food pellet consumption during the pretest in Groups TT, TL, LT, and BT was 61, 64, 57, and 54 pellets, respectively. There were no reliable differences among the groups. The center portion of Table 2 shows cup entry responding during the first tone, light, and pre-CS periods in Phase 2; the pattern of data seen at the end of Phase 1 was maintained except that responding to the tone in Group BT was much reduced. This reduction indicates that the high level of responding during the tone in Group BT during Phase I was not TABLE 2 Percentage Cup Responding in Experiment Phase I
Group Group Group Group
TT TL LT BT
I Phase 2, Trial 2
Phase 2, Trial I
Pre-CS
Tone
Light
Pre-CS
Tone
Light
Pre-CS
Tone
Light
4 3 4 7
55 51 8 71
6 6 32 8
3 4 3 6
50 54 6 14
4 6 30 4
3 2 0 2
34 32 3 6
2 4 20 I
b
PETER
C. HOLLAND
controlled by the tone itself, but was the result of prior food delivery. Responding was greater on the first Phase 2 tone trial in Group BT than in Group LT (U = 14) but this difference cannot unequivocally be attributed to backward conditioning since the actual time of food consumption was not under experimental control. The right portion of Table 2 shows responding during the second tone, light, and pre-CS periods in Phase 2, after a pairing of the tone with LiCl injection in Groups TT, LT, and BT, and a pairing of the light with the LiCl in Group TL. Of interest is a comparison of responding to the tone in Group TT and TL. If tone-LiCl pairings had direct effects on behavior evoked by the tone, these effects might be revealed as differences in cup responding on this trial. But responding did not differ between these two groups (U = 26). The primary data of Experiment 1 are the results of the food consumption test. Rats in Group TT, in which a representation of the food US was presumably paired with LiCl injection, consumed significantly fewer pellets (median = 7 1) than the rats in Group TL (median = 94; U = 11S), LT (median = 91; U = 15), and BT (median = 86, U = 16). The latter groups (in which such an evoked representation was not paired with illness) did not differ from each other. The increase in consumption between the pretest and the test was reliable in Groups TL, LT, and BT (Wilcoxon T’s c 5) but not in Group TT (T = 10). Considering the rising baseline of food consumption in the control groups (reflecting perhaps the increased familiarity with the test procedures), it is not surprising that tone-LiCl pairings in Group TT did not result in an actual decrease in consumption of the food US. But the lower consumption of Group TT relative to that in several control conditions demonstrates that tone-LiCl pairings can establish an aversion to a food previously paired with that tone. The explanation of that outcome favored here is that a representation or image of the food pellet US evoked by the tone was associated with the consequences of LiCl injection in Phase 2, just as Yaremko and Werner (1974) have claimed that imagined CSs and USs can be used to establish conditioning in human subjects. An alternate account for the data of Experiment 1 is that the reduced consumption in Group TT was mediated by illness-produced punishment of eating responses. The tone CS in Group TT may have evoked a number of consummatory behaviors; in Phase 2 LiCl injection may have punished those behaviors or conditioned competing behaviors to response feedback.
Experiments 2 and 3 examine the importance of response mediation in food aversions established in the manner of Experiment 1 by investigating the specificity of such food aversions. If the aversion established in procedures like those of Experiment 1 were mediated by responding evoked by the CS rather than a stimulus representation evoked by that
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7
CS, that averison would not be anticipated to be specific to the particular food substance involved (e.g., Trapold, 1970). EXPERIMENT 2 Experiment 2 examined the specificity of food aversions established by pairing a signal (CS) for food with LiCl injection. First, all rats received pairings of a tone CS with wintergreen-flavored food pellets and pairings of a light CS with a sucrose solution. Then separate groups of rats received LiCl injections immediately after presentation of the tone, the light, or neither CS. Finally, consumption of both the wintergreenflavored food pellets and sucrose solution was tested in all rats. Method Subjects and apparatus. The subjects were 24 female Sprague-Dawley rats about 100 days old at the beginning of the experiment. They were maintained at 80% of their normal body weights by rationing their food. Subjects were randomly assigned to three groups (n = 8). The apparatus was that used in Experiment I. Procedure. During the first 2 days, a pretest of the consumption of the two food substances was given in the rats’ homecages. All rats received 10 min access to a dish containing either 20 ml of 8% sucrose solution or 100 wintergreen-flavored food pellets like those used in Experiment 1. The order of presentation of the two foods was counterbalanced within each group. Phase I was designed to endow light and tone CSs with the ability to evoke quite different US representations. In each of the eight sessions of Phase I, all rats received four 10.5set presentations of the tone used in Experiment 1 terminating in delivery of two food pellets to the recessed food cups and four lo-set presentations of the flashing light used in Experiment 1 terminating in the delivery of 0.5 ml of the sucrose solution to the projecting food cup on the opposite wall. Session duration, intertrial intervals, and trial orders were identical to those used in Phase 1 of Experiment 1, During the next two days, another pretest of US consumption, identical to the first pretest, was administered to the rats in their homecages. Phase 2 was designed to establish an aversion to the representation of wintergreen food pellets in Group P, the representation of sucrose solution in Group S, or neither representation in Group C. In each session, the rats in all groups were placed in the experimental chambers for the usual 15min stimulus-free period. Then a single stimulus was presented; when that stimulus ended, the rats were immediately removed from the experimental chambers. On Days 1,4, and 5 of Phase 2, all rats in Group P and half of the rats in Group C received a 10.5-set tone CS accompanied by feeder operation (but not pellet delivery). The rats in Group P received
8
PETER
C. HOLLAND
injections of 0.3 M LiCl (0.5% body weight) as they were removed from the experimental chambers. On these days, the rats in Group S and the other half of the rats in Group C received a IO-set presentation of the light CS accompanied by dispenser operation (but not fluid delivery). The rats in Group S received LiCl injection immediately after light presentations. All rats in Group C were returned to their homecages after stimulus presentations and injected 4 hr later. On Days 2, 3, and 6 of Phase 2, all rats received a presentation of the stimulus not presented on Days I, 4, and 5 and were returned to their homecages without injection. During the next 2 days, a test of consumption of wintergreen pellets and sucrose solution was given in the rats’ homecages. As in the pretests, the rats were given 10 min access to either 100 wintergreen food pellets or 20 ml of the sucrose solution on alternate days. The order of presentation of the two food substances was counterbalanced within groups. Results Consumption of the wintergreen food pellets and sucrose solution was minimal during the first pretest (which occurred prior to Phase 1); over all rats, the median number of pellets consumed was 17 and the median amount of sucrose solution was 4 ml. These low levels of consumption might be attributable to the rats’ unfamiliarity with both the food substances and the consumption testing procedures. Responding to the recessed food cup during the tone CS which was paired with pellet delivery to that cup increased rapidly over the course of Phase I conditioning. Over the last two sessions, the percentages of cup responding during the tone were 58, 64, and 57% in Group P, S, and C, respectively. Responding to the recessed food cup was less than 10% during the light CS (which was paired with sucrose delivery to the other food cup) and during pre-CS periods in all groups. The results of the second consumption pretest (which occurred after Phase 1) are shown in the left portions of Fig. I. Mann-Whitney tests showed there were no reliable differences in pellet consumption among the groups (U’s 3 26.5); sucrose consumption also did not differ among the groups, although the difference between Group P and Group C approached significance (U = 16.5; U’s for other sucrose comparisons 3 21.5). Responding to the recessed food cup during the tone CS decreased rapidly over the course of Phase 2 training in all three groups. On the first tone presentation, the percentages of cup responding during the tone were 62,55, and 53% in Groups P, S, and C, respectively, but on the third (last) tone presentation, those percentages were 30,25, and 25%. There were no reiiable differences in responding to the tone among the groups at any point in Phase 2. Thus, tone-LiCl pairings had no measurable effect on
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PRETEST
s
P GROUPS
c
5
PRETEST
P
5 GROUPS
P
c
GROUPS
TEST
c
P
5 GROUPS
c
FIG. I. Results of the final pretest and test of sucrose consumption consumption (bottom) in Experiment 2.
(top) and pellet
responding to the tone itself. As in Phase I, rats did not respond to the recessed food cup during the light CS. The primary data of Experiment 2 are the results of the final food consumption test (right portions of Fig. I). Briefly, in Group S pairings of LiCl injection with a light CS previously associated with sucrose solution resulted in the establishment of an aversion to sucrose but not wintergreen pellets, and pairings of LiCl injection with tone CS presentations in Group P produced an averison to wintergreen pellets but not the sucrose solution. Sucrose consumption (top panel) was less in Group S than in either Group P (U = 15) or Group C (U = 5); Groups P and C did not differ reliably (U = 19.5). Conversely, consumption of the wintergreen food pellets (bottom panel) was significantly lower in Group P than in Group C (U = 13), and numerically (but not reliably, U = 16.5) lower than in Group S.
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Comparison of test and pretest data shows that differences in consumption patterns of Groups P and S in testing may have been obscured somewhat by the occurrence of opposite patterns in pretesting. To compensate for the (unreliable) preferences shown in pretesting, pretest-test difference scores (ds) were calculated for each subject. Sucrose consumption increased reliably between pretesting and testing in Group P (ds = -13.4, Wilcoxon T = 0) and Group C (ds = +3.5, T = 2), but decreased (although not significantly) in Group S (ds = -3.1, T = 8). These difference scores were reliably lower in Group S than in either Group P (U = 7) or Group C (I/ = 8), which did not differ from each other (U = 31.5). Food pellet consumption increased reliably in Group S (ds = +8.0, T = 3.5) and Group C (ds = + 14.5, T = 0) but decreased (but not significantly) in Group P (ds = -4.5, T = 8). These latter difference scores were reliably lower in Group P than in either Group S (U = 9.5) or Group C (U = 5), which did not reliably differ from each other (U = 18.5). The results of Experiment 2 extend those of Experiment 1: Aversions established by pairing LiCl injection with exteroceptive CSs were specific to the food substance previously associated with the devalued CS. Such specificity supports the view that the establishment of these aversions was mediated by stimulus representations of the food USs evoked by the CSs. However, these results do not rule out mediation by suppression of eating responses. Since the two food USs (and hence also the two CSs) probably evoked quite different approach and consummatory behaviors, CS-LiCl pairings may have resulted in suppression of conditioned approach and consummatory responses specific to the US previously associated with the devalued CS. Note, however, that the food cup entry CR recorded here was not measurably affected by CS-LiCl pairings: any response mediation would have to involve other, unrecorded responses such as chewing or licking. Experiment 3 examines the specificity of food aversions established in this manner when the two USs were likely to evoke identical approach and consummatory responses. EXPERIMENT 3 Experiment 3 further examined the specificity of food aversions established by pairing noxious events with CSs previously associated with food substances. Experiment 3 also compared the effectiveness of LiCl injection and electric shock in establishing food aversions in this manner. Each rat received two CSs separately paired with two food USs differing only in flavor. Then one of the CSs was paired with a noxious event, either shock or LiCl. Finally, consumption of the two food substances was assessed. Method Subjects and apparatus. The subjects were 16 male and 16 female Sprague-Dawley rats about 100 days old at the beginning of the experi-
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11
ment; sex was counterbalanced across all experimental conditions. The rats were food deprived so as to maintain them at 80% of their normal body weights. The apparatus was that used in Experiments 1 and 2. Procedure. Phase I was designed to endow tone and light CSs with the ability to evoke representations of food USs differing only in flavor. During each of the eight sessions of Phase 1, rats in Group P-Sh (n = 8) and Group P-Li (n = 8) received four IO.5set 1400-Hz tone CSs paired with delivery of two 45mg peppermint-flavored sucrose Pellets (P. J. Noyes Co.) and four 10.5set flashing (2/set) light CSs paired with delivery of two 45mg wintergreen-flavored sucrose Pellets. All pellets were delivered to the recessed food magazine; feeder operation occurred during the final 0.5 set of the CSs. The rats in Group F-Sh (n = 8) and Group F-Li (n = 8) received the same tone CSs paired with the delivery of 0.5 ml of a peppermint-flavored Fluid US and light CSs paired with the delivery of 0.5 ml of a wintergreen-flavored Fluid US. Both fluids were delivered to the projecting food cup during the 0. I-set interval beginning 10 set after CS onset. Thus, the CS remained on 0.4 set after operation of the fluid delivery devices. The fluid USs were made by dissolving 50 g of granulated wintergreen- or peppermint-flavored sucrose formula (P. J. Noyes Co.) in 1 liter of tap water. No attempt to match perceived intensities of pellet and fluid USs was made. Session durations, trial orders, and intertrial intervals were identical to those of Experiment 2. A pretest of consumption of the two USs received in Phase I was given in the rats’ homecages during the next two days. On each day, the rats in Groups P-Sh and P-Li received IO-min access to 100 wintergreen- or peppermint-flavored pellets; the rats in Groups F-Sh and F-Li received IO-min access to 20 ml of peppermint- or wintergreen-flavored fluids. The presentation order of the two flavored USs was counterbalanced within each group. Phase 2 was designed to establish an aversion to one of the USs (but not to the other) in all groups. In each session, rats received a single 10.5-set CS presentation (light or tone) in the experimental chambers after the usual 15-min stimulus-free period. Each CS was accompanied by the sound of the US delivery device (as in training) but no USs were delivered. On Days 1, 4, and 5 of Phase 2, one CS (light or tone, counterbalanced within each group) was paired with an aversive event. Rats in Groups P-Sh and F-S/z received a 0.5-set 0.5-mA grid shock during the last 0.5 set of CS presentations and were then returned to their homecages. Rats in Groups P-LI’ and F-LI’ were removed from the experimental chambers immediately after CS presentation, injected with 0.3 M LiCl (1% body weight), and then returned to their homecages. On Days 2, 3, and 6 of Phase 2 all rats received a presentation of the CS not delivered on Days 1, 4, and 5, and were returned to their homecages without receiving an aversive event.
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PETER C. HOLLAND
Next, all rats received a consumption test in the homecages identical to the consumption pretest. Finally, all rats received a consumption test in the experimental chambers. This test was identical to the homecage consumption tests except that the dishes were placed in the experimental chambers, fastened to the end wall not containing the reinforcement delivery devices. Results Responding to the recessed food cup during the tone and light CSs increased over the course of Phase 1 in Groups P-Sh and P-Li (which received pellets delivered to that food cup). In those groups combined, the percentages of cup responding during the tone CS, light CS, and pre-CS periods over the last two sessions of Phase 1 were 58,26, and 13%, respectively. Rats in Groups F-Sh and F-Li (which received fluid USs delivered to the projecting food cup) showed less than 5% responding to the recessed cup during pre-CS, light, or tone CS periods. Pretest consumption of the food substances whose CS-evoked representations were to be paired with an averison event or not in Phase 2 is shown in the left panels of Fig. 3. There were no reliable preferences for either one flavor over the other or for flavors to which an aversion would be trained versus those to which no aversion would be trained. CUP responding of Groups P-Sh and P-Li during the tone and light CSs in Phase 2 is shown in Fig. 2. On both the second and third tone trials, cup
00
TONE
CS
FIG. 2. Cup responding to the light CS (left) and the tone CS (right) in Groups P-Sh and P-Li in Phase 2 of Experiment 3. The solid symbols refer to responding evoked by CSs paired with shock (Sh) or LiCl injection (Li) in Phase 2 and the open symbols refer to responding evoked by CSs unpaired with shock or LiCl injection.
MEDIATED PRETEST D
Group F-L;
100
ll
D
N
N
Group F- Sh
PRETEST
I
D
Group P-b
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FOOD AVERSIONS
N
Group P-Sh
I I D
N
D
N
Group
Group
F-Li
F-Sh
D
N
Group P-U
TEST D
N
Group P-sh
FIG. 3. Results of the pretest and test of consumption in Groups F-Li and F-Sh (top) and Groups P-Li and P-Sh (bottom) in Experiment 3. The bars labeled D signify consumption of the substance whose CS-evoked representation was paired with a Devaluing agent in Phase 2; the bars labeled N indicate consumption of the substance whose CS-evoked representation was Not devalued in Phase 2.
responding in Group P-Sh was lower in the four rats that had received tone-shock pairings than in the four rats that had received light-shock pairings (U’s = 0). Cup responding to the light CS was lower in rats that had received iight-shock pairings than in rats that had received toneshock pairings (U’s = 0). Conversely, in Group P-Li there were no reliable differences in responding to either the light or tone CSs depending on whether or not the CS had been paired with LiCI. Thus, although CS-shock pairings rapidly produced suppression of cup behavior to those CSs, CS-LiCl pairings had no measurable direct effect on responding to the CSs. Consequently, responding to tone and light CSs paired with shock was lower than responding to those stimuli paired with LiCl (U’s c I) on the second and third presentation of each stimulus. The primary data of Experiment 3 are the results of the consumption
14
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test (right panels of Fig. 3). Rats consumed significantly less of the US which had its CS-evoked representation paired with LiCl-induced illness in Phase 2 than of the US whose representation had not been so paired in both Group F-Li (top right, Wilcoxon T = l), and Group P-Li (bottom right; T = 5). The results were similar regardless of whether signals for peppermint- or wintergreen-flavored USs were paired with LiCl in Phase 2. On the other hand, consumption of the food USs was not so affected in Groups F-Sh (T = 12.5) or Group P-Sh (T = 15) in which CS-evoked representations were paired with shock in Phase 2. Thus, CS-LiCl pairings selectively affected US consumption but CS-shock pairings did not. In fact, US consumption was greater in rats that received CS-shock pairings than in rats that received CS-LiCl pairings, for both those USs whose CS-evoked representations had been paired with the aversive event (Group P-Sh vs Group P-Li, U = 11.5; Group F-Sh vs Group F-Li, U = 0) and those USs whose representations had not been paired with the aversive event (Group P-Sh vs Group P-Li, U = 15.5; Group F-Sh vs Group F-Li, U = 10). Pretest-test difference scores were also calculated as in Experiment 2. CS-LiCI pairings reduced consumption of the US previously paired with that CS in seven of the eight rats in Group P-Li and in all of the rats in Group F-Li (sign test p’s s .035). CS-LiCI pairings reduced consumption of the US not previously associated with the LiCl-paired CS in only five of the eight rats in each of those groups (sign testp’s > 10). Further, in both Groups F-Li and P-Li, seven of eight rats showed greater decreases in consumption of the substance which had its CS-evoked representation paired with LiCl than in consumption of the substance whose CS-evoked representation had not been paired with LiCl. Conversely, CS-shock pairings did not result in reduced consumption of the food USs. Consumption of the US whose representation had been paired with shock decreased in only one rat in Group P-Sh and four rats in Group F-Sh; consumption of the other US decreased in only two rats and five rats in those groups, respectively. It is possible that the greater effects on food consumption of CS-LiCI than CS-shock pairings were the result of the rats’ experiencing illness but not shock or pain in the homecage (testing) environment. The final experimental chamber consumption tests permit an evaluation of that possibility. Median consumptions of the US associated with the CS previously devalued, and of the US associated with the CS not devalued, respectively, were 70 and 82 pellets in Group P-Li; 71 and 69 pellets in Group P-Sh; 11 and 15 ml in Group F-M; and 11 and 10 ml in Group F-Sh. The within-group preferences were reliable (T’s c 5) in both Group P-Li and Group F-Li, but not in Group P-Sh or Group F-Sh (T’s 2 12). Rats that received CS-shock pairings did in fact show less consumption of both devalued and undevalued USs in the experimental chambers than
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AVERSIONS
15
they did in the previous homecage tests (T’s < 3). Conversely, rats that received CS-LiCl pairings consumed more of the devalued US in the experimental chambers than in the homecages (T’s 6 5); it is not clear whether this difference reflects an effect of context or of test order. Consumption of the undevalued US did not differ reliably in the two tests (T’s 2 7) in the LiCl groups. As in the homecage consumption tests, rats that received CS-LiCl pairings preferred the food substance whose CS had not been devalued but rats that received CS-shock pairings did not show a similar specificity. The lack of specificity in the shocked rats suggests that reduced consumption in the experimental chamber test in those rats was more the result of fear conditioned to the chamber or other general suppressive factors than of an aversion conditioned to a US representation. In Experiment 3, specific food aversions were established by CS-LiCl pairings when the two food USs differed only in flavor. These results strongly suggest that aversions established by CS-LiCl pairings are mediated by detailed, CS-evoked representations of the food substances rather than by CS-evoked conditioned responses: it is hard to imagine that consummatory responding to those two USs could be so different as to mediate specific aversions. In additon, CS-shock pairings sufficient to suppress food cup entry more than did CS-LiCl pairings had no measurable specific effect on food consumption. Perhaps this contrast between shock and LiCl pairings reflects the frequently described ease of exteroceptive CS-shock association but difficulty of flavor-shock association (e.g., Garcia & Koelling, 1966). Or perhaps, shock was indeed associated with the flavor cues, but the consequent conditioned fear responses did not interfere with food consumption as it interfered with approach (see Jackson & Delprato, 1974). GENERAL DISCUSSION
The results of these experiments indicate that evoked representations of events can substitute for those events themselves in the formation of new associations. Rats developed flavor-specific aversions to food substances previously associated with exteroceptive CSs when those CSs were subsequently paired with LiCl, but not when those CSs were paired with shock. Mediation of these aversions by responses rather than by stimulus representations was unlikely. The procedures used to establish food aversions in these experiments resemble traditional sensory preconditioning procedures. In that design, as in the present experiments, two stimuli (A and B) are initially paired and then in a second phase one of them (B) receives conditioning. Finally, responding to the other stimulus (A) is assessed. Given suitable control conditions, responding to A is attributable to associations established
16
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C. HOLLAND
between A and B in Phase 1. (Since A and B are typically motivationally neutral in sensory preconditioning experiments, that design has frequently been used to address the question of whether associations can be formed between neutral events). The experiments reported here differed from typical sensory preconditioning experiments in two ways: first, the ordering of the A (food) and B (CSs) stimuli in Phase 1 correspond to a backward sensory preconditioning relation; second, in the present experiments, the formation of an association between the CSs and food in the first phase is not in question, rather concern is with how a CS-food association established in the first phase can mediate the establishment of the observed flavor aversion. Rescorla and Freberg (1978) suggested two ways in which associations established in sensory preconditioning procedures might mediate transfer of responding from one element to the other. One of those ways is identical to the mechanism for mediated aversions proposed here: associations established in Phase 1 endow B (CS) with the ability to activate a representation of A (food) during reinforced B training. Hence, A (food) may acquire a response directly by virtue of pairings of its representation with the US (LiCl) in the second phase. A second account is probably the more popular explanation of sensory preconditioning phenomena: A-B associations endow A with the ability to activate a representation of B during testing. Since reinforced B training established responding to B, A elicits responding indirectly by activating B’s representation. In the experiments reported here, perhaps in the test phase the food (A) activated a representation of the CS (B) previously paired with it via a backward association. If a rat had become averted to that CS in Phase 2 because of CS-LiCI (B-US) pairings then the particular food event might also evoke an aversion. Both accounts assume mediation of responding by an event representation evoked by another stimulus, but they differ in specifying the point in the experiment at which that mediation occurs. Only in the first account can such a representation be said to substitute for the event itself in the formation of new associations; in the second, more popular account, the representation is not conditioned, rather it merely evokes previously conditioned responding when activated. Considerable evidence within these experiments favors the first account (in which CS-food associations are used to activate a representation of food during the second, CS-LiCl pairing phase) over the second account (in which CS-food associations are used to evoke a representation of the CS during testing of food consumption.) First, since in the second account the ability of food to evoke a representation of the CS in testing is dependent on the formation of food-CS associations in the first phase, it would be reasonable to think that explicit food-tone pairings might especially encourage the development of food aversions in these
MEDIATED
FOOD
AVERSIONS
17
experiments. But in Experiment I, Group BT (which received food-tone pairings followed by tone-LiCl pairings) showed no evidence of a food aversion. Second, the second account demands the CS-LiCl pairings actually devalue the CS in some manner. But considerable data (e.g., Garcia & Koelling, 1966) suggest that auditory and visual stimuli are not particularly well associated with illness. In the present experiments, there was no evidence that tone or light CSs were devalued by pairings with LiCl. Further, when those CSs were measurably devalued by CS-shock pairings, there was no evidence that food aversions were established. The observation in Experiment 3 that CS-LiCl pairings were more effective in establishing food aversions but less effective in reducing responding to the CS itself thus suggests that the establishment of a food aversion in this manner depends mostly on conditioning of properties of the event representation evoked by the CS rather than on conditioning of an aversion to exteroceptive properties of the CS. It is important to note that, as in many sensory preconditioning experiments, the magnitude of the effects reported here was small. Typically in my laboratory two or three pairings of the food and LiCl substances used in these experiments would eliminate consumption entirely in testing. Yet here only small reductions in consumption or stable consumption compared to a rising baseline were observed. Similarly, devaluation of the food representation by CS-LiCL pairing was insufficient to affect cup responding to the CSs. Holland and Straub (1979) noted that devaluation of a food representation by food-LiCI pairings reduced the frequency of previously established food cup behavior to auditory CSs. In those experiments, however, responding to the CS was assessed after four pairings of food and LiCI, a manipulation which eliminated consumption of the food US. Given the small (but reliable) effect of two (Experiment I) or three (Experiments 2 and 3) CS-LiCl pairings on food consumption, it is not surprising that assessment of cup responding after only one or two such pairings in the experiments reported here did not reveal effects like those reported by Holland and Straub. At first glance, it would seem that the magnitude of these mediated aversions might be increased by more extensive CS-LiCl pairing or by making the consumption test more sensitive through more familiarization of the subjects with that procedure. But pilot data from my laboratory suggest that this is not the case, indeed, these preliminary data suggest that more extensive food preexposure or CS-LiCI pairings decrease the likelihood of observing mediated aversions. Rescorla and Freberg (1978) note analogous findings in sensory preconditioning: separate presentations of A and B tend to weaken sensory preconditioning effects, perhaps by degrading the A-B relation or by encouraging detrimental effects such as latent inhibition. I suspect that the small size of the aversions reported
18
PETER C. HOLLAND
here is not due merely to inadequacies of experimental design. Perhaps it indicates that CS-evoked representations of a US are distinguishable from the representation evoked by the US itself: they may be less salient or lack some features and hence generalize poorly to the representation evoked by the US itself. Nevertheless, the observed ability of detailed, evoked representations of stimulus events to substitute for their referents in the formation of new associations should increase our confidence in postulating the involvement of such representations in conditioning. REFERENCES Garcia, J., & Koelling,
R. A. Relation of cue to consequence in avoidance learning. Psychonomic Science, 1966, 4, 123-124. Holland, P. C. Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. Journal of Experimental Psychology: Animal Behavior Processes, 1977, 3, 77-104. Holland, P. C., & Rescorla, R. A. The effect of two ways of devaluing the unconditioned stimulus after first- and second-order appetitive conditioning. Journal ofExperimenra1 Psychology: Animal Behavior Processes, 1975, 1, 355-363. Holland, P. C., & Straub, J. J. Differential effects of two ways of devaluing the unconditioned stimulus after Pavlovian appetitive conditioning. Journa/ of Experimental Psychology: Animal Behavior Processes, 1979, 5, 65-78. Jackson, D. E.. & Delprato, D. J. Aversive CSs suppress lever pressing for food but not the eating of free food. Learning and Motivation, 1974, 5, 448-458. Konorski, J. Integrative activity in the brain. Chicago: Univ. of Chicago Press, 1967. Rescorla, R. A. A model of Pavlovian conditioning. In U. S. Rusinov (Ed.), Mechanisms of formation and inhibition of condifioned reflex. Moscow: Academy of Sciences of the USSR, 1974. Rescorla, R. A. Some cognitive approaches to conditioning. In S. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive processes in animal behavior. Hillsdale. N.J.: Erlbaum. 1978. Rescorla, R. A., & Freberg, L. The extinction of within-compound flavor associations. Learning and Motivation, 1978, 9, 41 l-427. Terry, W. S. Effects of priming unconditioned stimulus representation in short-term memory on Pavlovian conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 1976, 2, 354-369. Trapold, M. A. Are expectancies based upon different positive reinforcing events discriminably different? Learning and Motivation, 1970, 1, 129-140. Wagner, A. R. Expectancies and the priming of STM. In S. H. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive processes in animal behavior. Hillsdale, N.J.: Erlbaum. 1978. Yaremko, R. M., & Werner, M. Cognitive conditioning: Imagined stimulus contiguity and the third interval conditioned GSR. Pavlovian Journal of Biological Science, 1974. 9, 215-221. Received May 16, 1980 Revised August IO, 1980
AND
MOTIVATION
12, I-18 (1981)
Acquisition of Representation-Mediated Conditioned Food Aversions PETER C. HOLLAND University
of Pittsburgh
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-LiCI pairings showed less food consumption in subsequent testing than rats which received only tone-food or tone-LiCI 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 LiCI-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-UC1 pairings. These results suggest that CS-evoked representations of events can substitute for those events themselves in the formation of new associations.
Many recent theories presume the involvement of internal representations of the conditioned stimulus (CS) and the unconditioned stimulus (US) in Pavlovian conditioning. For instance, Konorski (1967) and Rescorla (1974) suggested that conditioned responding develops when the CS comes to activate a US representation which prior to conditioning could only be evoked by the US itself. The experiments reported here examined some of the properties of the US representations evoked by css. Considerable data support the claim that US representations are involved in the generation of conditioned responding. Rescorla and his colleagues for example (Holland & Rescorla, 1975; Rescorla, 1978) have performed a number of experiments in which the affective value of the US representation was modified after conditioning of a CS. Since conditioned This research was supported in part by Grant BNS 7903853 from the National Science Foundation. Thanks are due to Kathy Allen, who assisted in data collection in Experiment 3. Requests for reprints should be sent to Peter Holland, Department of Psychology, University of Pittsburgh, Pittsburgh. Pa. 15260. 0023-%90/81/010001-18$02.00/O Copyright @ 1981 by Academic Press. Inc. A11 rights of reproduction in any form resewed.
2
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C. HOLLAND
responding is presumably produced by activation of the US representation by the CS, modification of that representation should be reflected in subsequent responding to the CS. Responding to the CS was in fact observed to track postconditioned changes in US value in their experiments. Many theorists have assumed that in some respects activations of a US representation by either the US itself or by a CS are equivalent. For instance, Konorski (1967) attributed the frequently observed similarity of conditioned responses (CRs) and unconditioned responses (URs) to the fact that both responses are produced by activation of the same US representation. And Wagner and his colleagues (e.g., Terry, 1976; Wagner, 1978) found that various interference effects attributed to priming of a representation of the US into a short-term memory system occur whether that representation was primed directly by the US itself or was retrieved by a CS previously paired with that US. The experiments reported here examined the ability of a representation of an event retrieved from memory to substitute for that event itself in the formation of new associations involving that event. In Experiment I, an aversion to a food substance was produced by inducing illness immediately after the evocation of a representation of that food, in the absence of food itself. Experiments 2 and 3 examined the stimulus specificity of food aversions established in this manner. EXPERIMENT
1
In Experiment 1, a tone CS was repeatedly paired with food, presumably endowing that tone with the ability to evoke a representation of the food US. Then presentation of the tone alone was paired with the injection of an illness-inducing agent, lithium chloride. Finally, consumption of the food was tested. If the food representation evoked by the tone was sufficiently similar to the food US itself to enter into associations in a like manner, the tone-lithium chloride pairings might be anticipated to establish an aversion to that food, even though food itself was never paired with illness. Method Subjects. The subjects were 32 male Sprague-Dawley rats about 100 days old at the beginning of the experiment. They received unrestricted access to water but were deprived of food so as to maintain them at 80% of their ab lib weights. The rats were housed individually in stainless-steel cages measuring 17.8 x 25.4 x 17.8 cm. Apparatus. The experimental chambers consisted of eight identical chambers, 22.9 x 20.3 x 20.3 cm. Each chamber had a dimly illuminated, recessed food cup in the center of one end wall; these cups were fitted with photocells which activated circuitry in an adjoining room whenever a
MEDIATED
3
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rat’s head was inserted about 6 mm or more into the food cup. A similar food cup projected 3.7 cm into the chamber from the center of the other end wall; this cup was not used in Experiment I. To the left of the recessed food cup was an inoperative standard rat lever. The floor of the chamber was composed of 0.48-cm stainless-steel rods spaced 1.9 cm apart. The two end walls were aluminum; the side walls and top were clear acrylic plastic. Each chamber was enclosed in a light- and soundresistant closet. A speaker and a 6-W houselight were mounted on the inside wall of each closet enclosure, about IO cm above and in front of the experimental chamber. Procedure. An outline of the procedures of Experiment I is given in Table 1. Rats were randomly assigned to four groups of eight rats each and Phase I, designed to endow a tone CS with the ability to evoke a representation of food in some rats, was begun. In each of the eight daily sessions of Phase 1, rats in Groups TT and TL received four reinforced presentations of a 10.5set 1400-Hz (75 db SPL) tone and four nonreinforced presentations of a IO-set flashing (2/set) houselight. Rats in Group LT received four reinforced presentations of the IO.5set flashing houselight and four nonreinforced presentations of the IO-set 1400-Hz tone during each of these sessions. Rats in Group BT received four IO-set houselight CSs and four IO-set tone CSs in each Phase I session; reinforcements were delivered 5 set before each tone presentation. (The first letter of the group designations indicates whether rats received Tonefood, Light-food, or Backward food-tone pairings in Phase I .) The reinforcing event used in Phase 1 was the delivery of two 45-mg wintergreenflavored sucrose pellets (P. J. Noyes Co.) during the last 0.5 set of reinforced CSs. Feeder operation produced an audible click. Thus, at the end of Phase 1, the tone would be expected to evoke a representation of the wintergreen food pellets in Groups TT and TL, but not in Groups LT or BT. Each Phase 1 session was 75 min long; no trials were presented during the first 15 min of any session. Intertrial intervals averaged 7.5 min and were distributed rectangularly with a range of 4.5-10.5 min. Light and TABLE 1 Procedures of Experiment
I
Phase I Group Group Group Group
TT TL LT BT
T+fd,L+4 T-+ fd, L -+ 4 T-+q&L-+fd fd +T. L+ 4
Phase 2 Food Food Food Food
pretest pretest pretest pretest
T T T T
---) LiCI. + 4. L --, LiCI, -+ LiCI,
L + L L
-+ I$ LiCl -+ 4 -+ 4
Food Food Food Food
test test test test
Note. T, tone; L, light; 4, no explicit stimulus; fd, food; LiCI, lithium chloride injection.
groups were placed in the experimental chambers for the usual 15min stimulus-free period. Then a single stimulus was presented, immediately after which the rats were removed from the experimental chambers. On Days I and 3 of Phase 2, rats in Group TT received a 10.5set tone CS terminating in feeder operation (as in Phase l), but pellets were not delivered. Each rat was injected with 0.3 M lithium chloride (LiCl), 0.5% body weight, as it was removed from its experimental chamber. Because rats were run in squads of eight, the actual tone-injection interval ranged from 30 set to 5 min in each group. After the injections, each rat was placed in a small holding cage until all rats in that group had received injections; they were then returned to their homecages. Rats in Groups LT and BT received similar treatment except (as in Phase 1) the tone CS was 10 set long and was not accompanied by feeder operation. Rats in Group TL received similar injection treatment but received a IO-set light stimulus (unaccompanied by feeder operation) rather than the tone preceding each injection. (The second letter of the group designation indicates whether Tone or Light was paired with LiCl injection in Phase 2.) On Days 2 and 4 of Phase 2, rats in Groups TT and BT received a IO-set light stimulus; immediately after the light presentation the rats were placed in the holding cage for 5 min and then returned to their homecages. Rats in Group LT received similar treatment except the light was 10.5 set long and accompanied by feeder operation (but not pellet delivery). Rats in Group TL received a 10.5-set presentation of the tone accompanied by feeder operation (but not pellet delivery) on each of these 2 days. Thus, only the rats in Group TT had a CS-evoked representation of the food pellet US paired with LiCl injection. Finally, on the next day, all rats received a consumption test identical to the pretest of consumption described above. The primary data in these experiments were the number of food pellets consumed in the homecages during the various food consumption tests. In addition, food cup entries were recorded in the experimental apparatus. Output of the photocell circuits was interrogated at I-set intervals during the CS presentations and during the 30-set periods prior to CS presentations. The number of interrogations on which a rat had its head in the food
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cup during an interval was divided by the total number of interrogations during that interval to generate the measure “percentage cup responding.” This measure was selected as an index of conditioning since previous experiments (e.g., Holland, 1977) indicated that both auditory and visual CSs evoke food cup entry (magazine) behavior to some extent. Results Cup responding during reinforced CSs increased steadily over the course of Phase 1. The left side of Table 2 shows percentage cup responding during pre-CS, tone CS, and light CS intervals over the last two sessions. Every rat showed greater cup responding during the reinforced CS than during either the pre-CS period or the nonreinforced CS. Tone responding was reliably less in Group LT than in the other three groups (Mann-Whitney U’s c 8) which did not differ among themselves. The superiority of Groups TT and TL to Group LT indicated that the tone was conditioned in the former two groups. The superiority of Group BT, however, is likely to be more attributable to the rats’ consuming food pellets during CS presentations than to backward conditioning (see below). The percentage of cup responding during the light stimulus was greater in Group LT than in any of the other groups (U’s c 1 I), which did not differ from each other. The lower level of cup responding during the reinforced light CS than during the reinforced tone CSs probably reflects the occurrence of conditioned behavior to the localized light source (rearing) which is incompatible with the measured cup response (cf. Holland, 1977) rather than any substantial difference in the amount of conditioning. Pre-CS responding did not differ among the groups. Median food pellet consumption during the pretest in Groups TT, TL, LT, and BT was 61, 64, 57, and 54 pellets, respectively. There were no reliable differences among the groups. The center portion of Table 2 shows cup entry responding during the first tone, light, and pre-CS periods in Phase 2; the pattern of data seen at the end of Phase 1 was maintained except that responding to the tone in Group BT was much reduced. This reduction indicates that the high level of responding during the tone in Group BT during Phase I was not TABLE 2 Percentage Cup Responding in Experiment Phase I
Group Group Group Group
TT TL LT BT
I Phase 2, Trial 2
Phase 2, Trial I
Pre-CS
Tone
Light
Pre-CS
Tone
Light
Pre-CS
Tone
Light
4 3 4 7
55 51 8 71
6 6 32 8
3 4 3 6
50 54 6 14
4 6 30 4
3 2 0 2
34 32 3 6
2 4 20 I
b
PETER
C. HOLLAND
controlled by the tone itself, but was the result of prior food delivery. Responding was greater on the first Phase 2 tone trial in Group BT than in Group LT (U = 14) but this difference cannot unequivocally be attributed to backward conditioning since the actual time of food consumption was not under experimental control. The right portion of Table 2 shows responding during the second tone, light, and pre-CS periods in Phase 2, after a pairing of the tone with LiCl injection in Groups TT, LT, and BT, and a pairing of the light with the LiCl in Group TL. Of interest is a comparison of responding to the tone in Group TT and TL. If tone-LiCl pairings had direct effects on behavior evoked by the tone, these effects might be revealed as differences in cup responding on this trial. But responding did not differ between these two groups (U = 26). The primary data of Experiment 1 are the results of the food consumption test. Rats in Group TT, in which a representation of the food US was presumably paired with LiCl injection, consumed significantly fewer pellets (median = 7 1) than the rats in Group TL (median = 94; U = 11S), LT (median = 91; U = 15), and BT (median = 86, U = 16). The latter groups (in which such an evoked representation was not paired with illness) did not differ from each other. The increase in consumption between the pretest and the test was reliable in Groups TL, LT, and BT (Wilcoxon T’s c 5) but not in Group TT (T = 10). Considering the rising baseline of food consumption in the control groups (reflecting perhaps the increased familiarity with the test procedures), it is not surprising that tone-LiCl pairings in Group TT did not result in an actual decrease in consumption of the food US. But the lower consumption of Group TT relative to that in several control conditions demonstrates that tone-LiCl pairings can establish an aversion to a food previously paired with that tone. The explanation of that outcome favored here is that a representation or image of the food pellet US evoked by the tone was associated with the consequences of LiCl injection in Phase 2, just as Yaremko and Werner (1974) have claimed that imagined CSs and USs can be used to establish conditioning in human subjects. An alternate account for the data of Experiment 1 is that the reduced consumption in Group TT was mediated by illness-produced punishment of eating responses. The tone CS in Group TT may have evoked a number of consummatory behaviors; in Phase 2 LiCl injection may have punished those behaviors or conditioned competing behaviors to response feedback.
Experiments 2 and 3 examine the importance of response mediation in food aversions established in the manner of Experiment 1 by investigating the specificity of such food aversions. If the aversion established in procedures like those of Experiment 1 were mediated by responding evoked by the CS rather than a stimulus representation evoked by that
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7
CS, that averison would not be anticipated to be specific to the particular food substance involved (e.g., Trapold, 1970). EXPERIMENT 2 Experiment 2 examined the specificity of food aversions established by pairing a signal (CS) for food with LiCl injection. First, all rats received pairings of a tone CS with wintergreen-flavored food pellets and pairings of a light CS with a sucrose solution. Then separate groups of rats received LiCl injections immediately after presentation of the tone, the light, or neither CS. Finally, consumption of both the wintergreenflavored food pellets and sucrose solution was tested in all rats. Method Subjects and apparatus. The subjects were 24 female Sprague-Dawley rats about 100 days old at the beginning of the experiment. They were maintained at 80% of their normal body weights by rationing their food. Subjects were randomly assigned to three groups (n = 8). The apparatus was that used in Experiment I. Procedure. During the first 2 days, a pretest of the consumption of the two food substances was given in the rats’ homecages. All rats received 10 min access to a dish containing either 20 ml of 8% sucrose solution or 100 wintergreen-flavored food pellets like those used in Experiment 1. The order of presentation of the two foods was counterbalanced within each group. Phase I was designed to endow light and tone CSs with the ability to evoke quite different US representations. In each of the eight sessions of Phase I, all rats received four 10.5set presentations of the tone used in Experiment 1 terminating in delivery of two food pellets to the recessed food cups and four lo-set presentations of the flashing light used in Experiment 1 terminating in the delivery of 0.5 ml of the sucrose solution to the projecting food cup on the opposite wall. Session duration, intertrial intervals, and trial orders were identical to those used in Phase 1 of Experiment 1, During the next two days, another pretest of US consumption, identical to the first pretest, was administered to the rats in their homecages. Phase 2 was designed to establish an aversion to the representation of wintergreen food pellets in Group P, the representation of sucrose solution in Group S, or neither representation in Group C. In each session, the rats in all groups were placed in the experimental chambers for the usual 15min stimulus-free period. Then a single stimulus was presented; when that stimulus ended, the rats were immediately removed from the experimental chambers. On Days 1,4, and 5 of Phase 2, all rats in Group P and half of the rats in Group C received a 10.5-set tone CS accompanied by feeder operation (but not pellet delivery). The rats in Group P received
8
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C. HOLLAND
injections of 0.3 M LiCl (0.5% body weight) as they were removed from the experimental chambers. On these days, the rats in Group S and the other half of the rats in Group C received a IO-set presentation of the light CS accompanied by dispenser operation (but not fluid delivery). The rats in Group S received LiCl injection immediately after light presentations. All rats in Group C were returned to their homecages after stimulus presentations and injected 4 hr later. On Days 2, 3, and 6 of Phase 2, all rats received a presentation of the stimulus not presented on Days I, 4, and 5 and were returned to their homecages without injection. During the next 2 days, a test of consumption of wintergreen pellets and sucrose solution was given in the rats’ homecages. As in the pretests, the rats were given 10 min access to either 100 wintergreen food pellets or 20 ml of the sucrose solution on alternate days. The order of presentation of the two food substances was counterbalanced within groups. Results Consumption of the wintergreen food pellets and sucrose solution was minimal during the first pretest (which occurred prior to Phase 1); over all rats, the median number of pellets consumed was 17 and the median amount of sucrose solution was 4 ml. These low levels of consumption might be attributable to the rats’ unfamiliarity with both the food substances and the consumption testing procedures. Responding to the recessed food cup during the tone CS which was paired with pellet delivery to that cup increased rapidly over the course of Phase I conditioning. Over the last two sessions, the percentages of cup responding during the tone were 58, 64, and 57% in Group P, S, and C, respectively. Responding to the recessed food cup was less than 10% during the light CS (which was paired with sucrose delivery to the other food cup) and during pre-CS periods in all groups. The results of the second consumption pretest (which occurred after Phase 1) are shown in the left portions of Fig. I. Mann-Whitney tests showed there were no reliable differences in pellet consumption among the groups (U’s 3 26.5); sucrose consumption also did not differ among the groups, although the difference between Group P and Group C approached significance (U = 16.5; U’s for other sucrose comparisons 3 21.5). Responding to the recessed food cup during the tone CS decreased rapidly over the course of Phase 2 training in all three groups. On the first tone presentation, the percentages of cup responding during the tone were 62,55, and 53% in Groups P, S, and C, respectively, but on the third (last) tone presentation, those percentages were 30,25, and 25%. There were no reiiable differences in responding to the tone among the groups at any point in Phase 2. Thus, tone-LiCl pairings had no measurable effect on
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PRETEST
s
P GROUPS
c
5
PRETEST
P
5 GROUPS
P
c
GROUPS
TEST
c
P
5 GROUPS
c
FIG. I. Results of the final pretest and test of sucrose consumption consumption (bottom) in Experiment 2.
(top) and pellet
responding to the tone itself. As in Phase I, rats did not respond to the recessed food cup during the light CS. The primary data of Experiment 2 are the results of the final food consumption test (right portions of Fig. I). Briefly, in Group S pairings of LiCl injection with a light CS previously associated with sucrose solution resulted in the establishment of an aversion to sucrose but not wintergreen pellets, and pairings of LiCl injection with tone CS presentations in Group P produced an averison to wintergreen pellets but not the sucrose solution. Sucrose consumption (top panel) was less in Group S than in either Group P (U = 15) or Group C (U = 5); Groups P and C did not differ reliably (U = 19.5). Conversely, consumption of the wintergreen food pellets (bottom panel) was significantly lower in Group P than in Group C (U = 13), and numerically (but not reliably, U = 16.5) lower than in Group S.
10
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C. HOLLAND
Comparison of test and pretest data shows that differences in consumption patterns of Groups P and S in testing may have been obscured somewhat by the occurrence of opposite patterns in pretesting. To compensate for the (unreliable) preferences shown in pretesting, pretest-test difference scores (ds) were calculated for each subject. Sucrose consumption increased reliably between pretesting and testing in Group P (ds = -13.4, Wilcoxon T = 0) and Group C (ds = +3.5, T = 2), but decreased (although not significantly) in Group S (ds = -3.1, T = 8). These difference scores were reliably lower in Group S than in either Group P (U = 7) or Group C (I/ = 8), which did not differ from each other (U = 31.5). Food pellet consumption increased reliably in Group S (ds = +8.0, T = 3.5) and Group C (ds = + 14.5, T = 0) but decreased (but not significantly) in Group P (ds = -4.5, T = 8). These latter difference scores were reliably lower in Group P than in either Group S (U = 9.5) or Group C (U = 5), which did not reliably differ from each other (U = 18.5). The results of Experiment 2 extend those of Experiment 1: Aversions established by pairing LiCl injection with exteroceptive CSs were specific to the food substance previously associated with the devalued CS. Such specificity supports the view that the establishment of these aversions was mediated by stimulus representations of the food USs evoked by the CSs. However, these results do not rule out mediation by suppression of eating responses. Since the two food USs (and hence also the two CSs) probably evoked quite different approach and consummatory behaviors, CS-LiCl pairings may have resulted in suppression of conditioned approach and consummatory responses specific to the US previously associated with the devalued CS. Note, however, that the food cup entry CR recorded here was not measurably affected by CS-LiCl pairings: any response mediation would have to involve other, unrecorded responses such as chewing or licking. Experiment 3 examines the specificity of food aversions established in this manner when the two USs were likely to evoke identical approach and consummatory responses. EXPERIMENT 3 Experiment 3 further examined the specificity of food aversions established by pairing noxious events with CSs previously associated with food substances. Experiment 3 also compared the effectiveness of LiCl injection and electric shock in establishing food aversions in this manner. Each rat received two CSs separately paired with two food USs differing only in flavor. Then one of the CSs was paired with a noxious event, either shock or LiCl. Finally, consumption of the two food substances was assessed. Method Subjects and apparatus. The subjects were 16 male and 16 female Sprague-Dawley rats about 100 days old at the beginning of the experi-
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11
ment; sex was counterbalanced across all experimental conditions. The rats were food deprived so as to maintain them at 80% of their normal body weights. The apparatus was that used in Experiments 1 and 2. Procedure. Phase I was designed to endow tone and light CSs with the ability to evoke representations of food USs differing only in flavor. During each of the eight sessions of Phase 1, rats in Group P-Sh (n = 8) and Group P-Li (n = 8) received four IO.5set 1400-Hz tone CSs paired with delivery of two 45mg peppermint-flavored sucrose Pellets (P. J. Noyes Co.) and four 10.5set flashing (2/set) light CSs paired with delivery of two 45mg wintergreen-flavored sucrose Pellets. All pellets were delivered to the recessed food magazine; feeder operation occurred during the final 0.5 set of the CSs. The rats in Group F-Sh (n = 8) and Group F-Li (n = 8) received the same tone CSs paired with the delivery of 0.5 ml of a peppermint-flavored Fluid US and light CSs paired with the delivery of 0.5 ml of a wintergreen-flavored Fluid US. Both fluids were delivered to the projecting food cup during the 0. I-set interval beginning 10 set after CS onset. Thus, the CS remained on 0.4 set after operation of the fluid delivery devices. The fluid USs were made by dissolving 50 g of granulated wintergreen- or peppermint-flavored sucrose formula (P. J. Noyes Co.) in 1 liter of tap water. No attempt to match perceived intensities of pellet and fluid USs was made. Session durations, trial orders, and intertrial intervals were identical to those of Experiment 2. A pretest of consumption of the two USs received in Phase I was given in the rats’ homecages during the next two days. On each day, the rats in Groups P-Sh and P-Li received IO-min access to 100 wintergreen- or peppermint-flavored pellets; the rats in Groups F-Sh and F-Li received IO-min access to 20 ml of peppermint- or wintergreen-flavored fluids. The presentation order of the two flavored USs was counterbalanced within each group. Phase 2 was designed to establish an aversion to one of the USs (but not to the other) in all groups. In each session, rats received a single 10.5-set CS presentation (light or tone) in the experimental chambers after the usual 15-min stimulus-free period. Each CS was accompanied by the sound of the US delivery device (as in training) but no USs were delivered. On Days 1, 4, and 5 of Phase 2, one CS (light or tone, counterbalanced within each group) was paired with an aversive event. Rats in Groups P-Sh and F-S/z received a 0.5-set 0.5-mA grid shock during the last 0.5 set of CS presentations and were then returned to their homecages. Rats in Groups P-LI’ and F-LI’ were removed from the experimental chambers immediately after CS presentation, injected with 0.3 M LiCl (1% body weight), and then returned to their homecages. On Days 2, 3, and 6 of Phase 2 all rats received a presentation of the CS not delivered on Days 1, 4, and 5, and were returned to their homecages without receiving an aversive event.
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Next, all rats received a consumption test in the homecages identical to the consumption pretest. Finally, all rats received a consumption test in the experimental chambers. This test was identical to the homecage consumption tests except that the dishes were placed in the experimental chambers, fastened to the end wall not containing the reinforcement delivery devices. Results Responding to the recessed food cup during the tone and light CSs increased over the course of Phase 1 in Groups P-Sh and P-Li (which received pellets delivered to that food cup). In those groups combined, the percentages of cup responding during the tone CS, light CS, and pre-CS periods over the last two sessions of Phase 1 were 58,26, and 13%, respectively. Rats in Groups F-Sh and F-Li (which received fluid USs delivered to the projecting food cup) showed less than 5% responding to the recessed cup during pre-CS, light, or tone CS periods. Pretest consumption of the food substances whose CS-evoked representations were to be paired with an averison event or not in Phase 2 is shown in the left panels of Fig. 3. There were no reliable preferences for either one flavor over the other or for flavors to which an aversion would be trained versus those to which no aversion would be trained. CUP responding of Groups P-Sh and P-Li during the tone and light CSs in Phase 2 is shown in Fig. 2. On both the second and third tone trials, cup
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FIG. 2. Cup responding to the light CS (left) and the tone CS (right) in Groups P-Sh and P-Li in Phase 2 of Experiment 3. The solid symbols refer to responding evoked by CSs paired with shock (Sh) or LiCl injection (Li) in Phase 2 and the open symbols refer to responding evoked by CSs unpaired with shock or LiCl injection.
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Group F-L;
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FIG. 3. Results of the pretest and test of consumption in Groups F-Li and F-Sh (top) and Groups P-Li and P-Sh (bottom) in Experiment 3. The bars labeled D signify consumption of the substance whose CS-evoked representation was paired with a Devaluing agent in Phase 2; the bars labeled N indicate consumption of the substance whose CS-evoked representation was Not devalued in Phase 2.
responding in Group P-Sh was lower in the four rats that had received tone-shock pairings than in the four rats that had received light-shock pairings (U’s = 0). Cup responding to the light CS was lower in rats that had received iight-shock pairings than in rats that had received toneshock pairings (U’s = 0). Conversely, in Group P-Li there were no reliable differences in responding to either the light or tone CSs depending on whether or not the CS had been paired with LiCI. Thus, although CS-shock pairings rapidly produced suppression of cup behavior to those CSs, CS-LiCl pairings had no measurable direct effect on responding to the CSs. Consequently, responding to tone and light CSs paired with shock was lower than responding to those stimuli paired with LiCl (U’s c I) on the second and third presentation of each stimulus. The primary data of Experiment 3 are the results of the consumption
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test (right panels of Fig. 3). Rats consumed significantly less of the US which had its CS-evoked representation paired with LiCl-induced illness in Phase 2 than of the US whose representation had not been so paired in both Group F-Li (top right, Wilcoxon T = l), and Group P-Li (bottom right; T = 5). The results were similar regardless of whether signals for peppermint- or wintergreen-flavored USs were paired with LiCl in Phase 2. On the other hand, consumption of the food USs was not so affected in Groups F-Sh (T = 12.5) or Group P-Sh (T = 15) in which CS-evoked representations were paired with shock in Phase 2. Thus, CS-LiCl pairings selectively affected US consumption but CS-shock pairings did not. In fact, US consumption was greater in rats that received CS-shock pairings than in rats that received CS-LiCl pairings, for both those USs whose CS-evoked representations had been paired with the aversive event (Group P-Sh vs Group P-Li, U = 11.5; Group F-Sh vs Group F-Li, U = 0) and those USs whose representations had not been paired with the aversive event (Group P-Sh vs Group P-Li, U = 15.5; Group F-Sh vs Group F-Li, U = 10). Pretest-test difference scores were also calculated as in Experiment 2. CS-LiCI pairings reduced consumption of the US previously paired with that CS in seven of the eight rats in Group P-Li and in all of the rats in Group F-Li (sign test p’s s .035). CS-LiCI pairings reduced consumption of the US not previously associated with the LiCl-paired CS in only five of the eight rats in each of those groups (sign testp’s > 10). Further, in both Groups F-Li and P-Li, seven of eight rats showed greater decreases in consumption of the substance which had its CS-evoked representation paired with LiCl than in consumption of the substance whose CS-evoked representation had not been paired with LiCl. Conversely, CS-shock pairings did not result in reduced consumption of the food USs. Consumption of the US whose representation had been paired with shock decreased in only one rat in Group P-Sh and four rats in Group F-Sh; consumption of the other US decreased in only two rats and five rats in those groups, respectively. It is possible that the greater effects on food consumption of CS-LiCI than CS-shock pairings were the result of the rats’ experiencing illness but not shock or pain in the homecage (testing) environment. The final experimental chamber consumption tests permit an evaluation of that possibility. Median consumptions of the US associated with the CS previously devalued, and of the US associated with the CS not devalued, respectively, were 70 and 82 pellets in Group P-Li; 71 and 69 pellets in Group P-Sh; 11 and 15 ml in Group F-M; and 11 and 10 ml in Group F-Sh. The within-group preferences were reliable (T’s c 5) in both Group P-Li and Group F-Li, but not in Group P-Sh or Group F-Sh (T’s 2 12). Rats that received CS-shock pairings did in fact show less consumption of both devalued and undevalued USs in the experimental chambers than
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they did in the previous homecage tests (T’s < 3). Conversely, rats that received CS-LiCl pairings consumed more of the devalued US in the experimental chambers than in the homecages (T’s 6 5); it is not clear whether this difference reflects an effect of context or of test order. Consumption of the undevalued US did not differ reliably in the two tests (T’s 2 7) in the LiCl groups. As in the homecage consumption tests, rats that received CS-LiCl pairings preferred the food substance whose CS had not been devalued but rats that received CS-shock pairings did not show a similar specificity. The lack of specificity in the shocked rats suggests that reduced consumption in the experimental chamber test in those rats was more the result of fear conditioned to the chamber or other general suppressive factors than of an aversion conditioned to a US representation. In Experiment 3, specific food aversions were established by CS-LiCl pairings when the two food USs differed only in flavor. These results strongly suggest that aversions established by CS-LiCl pairings are mediated by detailed, CS-evoked representations of the food substances rather than by CS-evoked conditioned responses: it is hard to imagine that consummatory responding to those two USs could be so different as to mediate specific aversions. In additon, CS-shock pairings sufficient to suppress food cup entry more than did CS-LiCl pairings had no measurable specific effect on food consumption. Perhaps this contrast between shock and LiCl pairings reflects the frequently described ease of exteroceptive CS-shock association but difficulty of flavor-shock association (e.g., Garcia & Koelling, 1966). Or perhaps, shock was indeed associated with the flavor cues, but the consequent conditioned fear responses did not interfere with food consumption as it interfered with approach (see Jackson & Delprato, 1974). GENERAL DISCUSSION
The results of these experiments indicate that evoked representations of events can substitute for those events themselves in the formation of new associations. Rats developed flavor-specific aversions to food substances previously associated with exteroceptive CSs when those CSs were subsequently paired with LiCl, but not when those CSs were paired with shock. Mediation of these aversions by responses rather than by stimulus representations was unlikely. The procedures used to establish food aversions in these experiments resemble traditional sensory preconditioning procedures. In that design, as in the present experiments, two stimuli (A and B) are initially paired and then in a second phase one of them (B) receives conditioning. Finally, responding to the other stimulus (A) is assessed. Given suitable control conditions, responding to A is attributable to associations established
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between A and B in Phase 1. (Since A and B are typically motivationally neutral in sensory preconditioning experiments, that design has frequently been used to address the question of whether associations can be formed between neutral events). The experiments reported here differed from typical sensory preconditioning experiments in two ways: first, the ordering of the A (food) and B (CSs) stimuli in Phase 1 correspond to a backward sensory preconditioning relation; second, in the present experiments, the formation of an association between the CSs and food in the first phase is not in question, rather concern is with how a CS-food association established in the first phase can mediate the establishment of the observed flavor aversion. Rescorla and Freberg (1978) suggested two ways in which associations established in sensory preconditioning procedures might mediate transfer of responding from one element to the other. One of those ways is identical to the mechanism for mediated aversions proposed here: associations established in Phase 1 endow B (CS) with the ability to activate a representation of A (food) during reinforced B training. Hence, A (food) may acquire a response directly by virtue of pairings of its representation with the US (LiCl) in the second phase. A second account is probably the more popular explanation of sensory preconditioning phenomena: A-B associations endow A with the ability to activate a representation of B during testing. Since reinforced B training established responding to B, A elicits responding indirectly by activating B’s representation. In the experiments reported here, perhaps in the test phase the food (A) activated a representation of the CS (B) previously paired with it via a backward association. If a rat had become averted to that CS in Phase 2 because of CS-LiCI (B-US) pairings then the particular food event might also evoke an aversion. Both accounts assume mediation of responding by an event representation evoked by another stimulus, but they differ in specifying the point in the experiment at which that mediation occurs. Only in the first account can such a representation be said to substitute for the event itself in the formation of new associations; in the second, more popular account, the representation is not conditioned, rather it merely evokes previously conditioned responding when activated. Considerable evidence within these experiments favors the first account (in which CS-food associations are used to activate a representation of food during the second, CS-LiCl pairing phase) over the second account (in which CS-food associations are used to evoke a representation of the CS during testing of food consumption.) First, since in the second account the ability of food to evoke a representation of the CS in testing is dependent on the formation of food-CS associations in the first phase, it would be reasonable to think that explicit food-tone pairings might especially encourage the development of food aversions in these
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experiments. But in Experiment I, Group BT (which received food-tone pairings followed by tone-LiCl pairings) showed no evidence of a food aversion. Second, the second account demands the CS-LiCl pairings actually devalue the CS in some manner. But considerable data (e.g., Garcia & Koelling, 1966) suggest that auditory and visual stimuli are not particularly well associated with illness. In the present experiments, there was no evidence that tone or light CSs were devalued by pairings with LiCl. Further, when those CSs were measurably devalued by CS-shock pairings, there was no evidence that food aversions were established. The observation in Experiment 3 that CS-LiCl pairings were more effective in establishing food aversions but less effective in reducing responding to the CS itself thus suggests that the establishment of a food aversion in this manner depends mostly on conditioning of properties of the event representation evoked by the CS rather than on conditioning of an aversion to exteroceptive properties of the CS. It is important to note that, as in many sensory preconditioning experiments, the magnitude of the effects reported here was small. Typically in my laboratory two or three pairings of the food and LiCl substances used in these experiments would eliminate consumption entirely in testing. Yet here only small reductions in consumption or stable consumption compared to a rising baseline were observed. Similarly, devaluation of the food representation by CS-LiCL pairing was insufficient to affect cup responding to the CSs. Holland and Straub (1979) noted that devaluation of a food representation by food-LiCI pairings reduced the frequency of previously established food cup behavior to auditory CSs. In those experiments, however, responding to the CS was assessed after four pairings of food and LiCI, a manipulation which eliminated consumption of the food US. Given the small (but reliable) effect of two (Experiment I) or three (Experiments 2 and 3) CS-LiCl pairings on food consumption, it is not surprising that assessment of cup responding after only one or two such pairings in the experiments reported here did not reveal effects like those reported by Holland and Straub. At first glance, it would seem that the magnitude of these mediated aversions might be increased by more extensive CS-LiCl pairing or by making the consumption test more sensitive through more familiarization of the subjects with that procedure. But pilot data from my laboratory suggest that this is not the case, indeed, these preliminary data suggest that more extensive food preexposure or CS-LiCI pairings decrease the likelihood of observing mediated aversions. Rescorla and Freberg (1978) note analogous findings in sensory preconditioning: separate presentations of A and B tend to weaken sensory preconditioning effects, perhaps by degrading the A-B relation or by encouraging detrimental effects such as latent inhibition. I suspect that the small size of the aversions reported
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here is not due merely to inadequacies of experimental design. Perhaps it indicates that CS-evoked representations of a US are distinguishable from the representation evoked by the US itself: they may be less salient or lack some features and hence generalize poorly to the representation evoked by the US itself. Nevertheless, the observed ability of detailed, evoked representations of stimulus events to substitute for their referents in the formation of new associations should increase our confidence in postulating the involvement of such representations in conditioning. REFERENCES Garcia, J., & Koelling,
R. A. Relation of cue to consequence in avoidance learning. Psychonomic Science, 1966, 4, 123-124. Holland, P. C. Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. Journal of Experimental Psychology: Animal Behavior Processes, 1977, 3, 77-104. Holland, P. C., & Rescorla, R. A. The effect of two ways of devaluing the unconditioned stimulus after first- and second-order appetitive conditioning. Journal ofExperimenra1 Psychology: Animal Behavior Processes, 1975, 1, 355-363. Holland, P. C., & Straub, J. J. Differential effects of two ways of devaluing the unconditioned stimulus after Pavlovian appetitive conditioning. Journa/ of Experimental Psychology: Animal Behavior Processes, 1979, 5, 65-78. Jackson, D. E.. & Delprato, D. J. Aversive CSs suppress lever pressing for food but not the eating of free food. Learning and Motivation, 1974, 5, 448-458. Konorski, J. Integrative activity in the brain. Chicago: Univ. of Chicago Press, 1967. Rescorla, R. A. A model of Pavlovian conditioning. In U. S. Rusinov (Ed.), Mechanisms of formation and inhibition of condifioned reflex. Moscow: Academy of Sciences of the USSR, 1974. Rescorla, R. A. Some cognitive approaches to conditioning. In S. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive processes in animal behavior. Hillsdale. N.J.: Erlbaum. 1978. Rescorla, R. A., & Freberg, L. The extinction of within-compound flavor associations. Learning and Motivation, 1978, 9, 41 l-427. Terry, W. S. Effects of priming unconditioned stimulus representation in short-term memory on Pavlovian conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 1976, 2, 354-369. Trapold, M. A. Are expectancies based upon different positive reinforcing events discriminably different? Learning and Motivation, 1970, 1, 129-140. Wagner, A. R. Expectancies and the priming of STM. In S. H. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive processes in animal behavior. Hillsdale, N.J.: Erlbaum. 1978. Yaremko, R. M., & Werner, M. Cognitive conditioning: Imagined stimulus contiguity and the third interval conditioned GSR. Pavlovian Journal of Biological Science, 1974. 9, 215-221. Received May 16, 1980 Revised August IO, 1980