PSYCHOLOGICAL SCIENCE
Research Article
INHIBITION AND SUPERCONDITIONING
Ben A. Williams1 and Margaret A. McDevitt2
1
University of California, San Diego, and 2Western Maryland College
Abstract—Superconditioning is said to occur when learning an association between a conditioned stimulus (CS) and unconditioned stimulus (US) is facilitated by pairing the CS with the US in the presence of
a previously established conditioned inhibitor. Previous demonstrations of superconditioning have been criticized because their control
conditions have allowed alternative interpretations. Using a withinsubjects autoshaping procedure, the present study unambiguously demonstrated superconditioning. The results support the view that superconditioning is the symmetric opposite of blocking.
The concept of inhibition has played an important role in the history of behavior theory. The discovery of inhibition as a distinct aspect
of the nervous system inspired Sechenov in 1868 to attempt to explain
all mental functions in terms of reflexology. For Pavlov, inhibition was
an even more important concept than excitation, as he distinguished
between several different kinds of inhibition and in his later years
speculated that much mental illness is due to the malfunction of general inhibitory processes (see Boakes, 1984, for discussion of both
Sechenov and Pavlov). In contrast to the Russians, American behaviorists have viewed inhibition as a concept of questionable validity.
Although Spence (1936, 1937) invoked the concept as an essential part
of his account of discrimination learning, Watson, Guthrie, Thorndike,
and Tolman never entertained the concept. Skinner (1938, p. 96) acknowledged the metaphorical value of the concept but disputed whether
there is an inhibitory process that actively suppresses behavior. It was
not until the renewed appreciation of Konorski (1948, 1967) in the
1960s that inhibition received extensive attention, culminating in the
conditioning model of Rescorla and Wagner (1972), which assumed
that inhibitory conditioning is the symmetric opposite of excitatory
conditioning.
The idea that inhibition is the symmetric opposite of excitation is
now strongly disputed (see Savastano, Cole, Barnet, & Miller, 1999,
for a recent review). Rescorla (1985) argued that inhibition is instead
the symmetric opposite of facilitation and that both inhibition and facilitation are forms of occasion setting by which stimuli modulate the
threshold of activation of the representation of the unconditioned stimulus (US). Accordingly, both types of occasion setting are qualitatively different from the association between the conditioned stimulus
(CS) and US that underlies conditioned excitation.
A further challenge to the concept of inhibitory associations has
come from the comparator theories of Gibbon and Balsam (1981) and
Miller and Matzel (1988), which assert that inhibitory associations do
not exist. Instead, there are only different degrees of excitatory associations and a comparison between levels of association. Accordingly,
experimental results that indicate that a stimulus (the nominal CS)
has acquired conditioned inhibitory properties reflect not a learning
effect but a performance effect generated by this comparison process.
Address correspondence to Ben A. Williams, Department of Psychology,
University of California, San Diego, La Jolla, CA 92093-0109; e-mail: bawilliams
@ucsd.edu.
454
Copyright © 2002 American Psychological Society
Essential to the idea of an inhibitory association is that the CS
predicts the absence of the US. Thus, a conditioned inhibitor reduces
responding in a summation test (in which a conditioned excitor, CS,
and a CS are presented together) because its negative association with
the US counteracts the prediction of impending US presentation due
to the CS. But as noted, the empirical demonstration of conditioned
inhibition has interpretations that do not rely on negative associations
per se.
Some insight into the theoretical interpretation of the empirical
phenomenon of conditioned inhibition perhaps can be provided by establishing the extent to which conditioned inhibitors share the property of conditioned excitors of modulating the degree of conditioning
to other stimuli that are trained in their presence. The discovery of
blocking (Kamin, 1968, 1969) demonstrated that conditioning to a
novel stimulus due to pairing with a US will be attenuated if a previously trained CS is presented in compound with that novel stimulus.
The presumed basis of blocking has been that the novel stimulus provides no new information, and therefore no conditioning to it occurs.
Thus, conditioning occurs to a new CS only to the extent that the subject is “surprised” by the occurrence of the US.
The issue addressed by the present study is whether an effect symmetrically opposite to blocking occurs when a stimulus compound of
a pretrained conditioned inhibitor with a novel CS is paired with the
US. Such an effect should be expected if the CS predicts the absence
of the US, so that US presentation is even less expected in the presence of the CS than if the novel CS had been presented alone at the
time of US presentation. A greater amount of conditioning therefore
accrues to the novel CS, given the assumption that the amount of
learning is a function of the extent to which the US presentation is not
expected. Such a finding has been labeled superconditioning in recognition of the enhanced conditioning that the presence of a CS produces.
In comparison with blocking, for which there has been voluminous
research, superconditioning has received relatively little investigation.
Several studies have reported enhanced conditioning when a previously established CS was presented in compound with a new CS
(Blanchard & Honig, 1976; Rescorla, 1971; Wagner, 1971). However,
Navarro, Hallam, Matzel, and Miller (1989) disputed whether superconditioning is a reliable empirical finding. They argued that the supposedly enhanced learning that had been reported in previous studies
was actually an artifact of using a control condition in which the novel
CS was presented in compound with a second CS with no prior history. This control condition is inadequate, they said, because training a
stimulus to become a CS causes it to lose attentional salience. This
loss of salience causes the stimulus trained as the CS to have less attention value than the novel CS when the CS and novel CS are presented in compound. In the control condition, however, the target
stimulus and the second CS with which it is compounded are equally
salient. Because elements of a compound stimulus mutually compete
for stimulus control (a phenomenon known as overshadowing), the
greater degree of conditioning to the novel CS in compound with the
CS could be due to less overshadowing rather than enhanced learnVOL. 13, NO. 5, SEPTEMBER 2002
PSYCHOLOGICAL SCIENCE
Ben A. Williams and Margaret A. McDevitt
ing to the novel CS. Accordingly, in their own study, Navarro et al.
included a second control condition in which the novel CS was conditioned when presented alone. They reported that the amount of learning in the superconditioning condition was not enhanced relative to
this alternative control condition.
The assumption of Navarro et al. (1989) that conditioned inhibition
training produces a loss of attention salience for the CS is challenged by the fact that conditioned inhibitors suppress behavior more
effectively in summation tests than do novel stimuli. If conditioned inhibition training caused the CS to lose salience, this should be reflected in a weaker ability to suppress ongoing behavior. The generality
of their results may also be questioned because of their use of the explicitly unpaired procedure as a method of establishing conditioned
inhibition in three of their four experiments. Explicitly unpaired training is known to produce weaker conditioned inhibition than the more
standard A/AB procedure, in which the CS is alternated in a discrimination procedure with the compound of the CS and CS. Experiment 4 of Navarro et al. did use the more conventional conditioned
inhibition training procedure, and nevertheless failed to demonstrate
superconditioning. It should be noted, however, that the test conditions were less subject to generalization decrements for the control
subjects than for those in the superconditioning group, because all
subjects were tested with the target CS in isolation. Moreover, Pearce
and Redhead (1995) did produce a form of superconditioning not susceptible to the criticisms of Navarro et al., although they interpreted
their results in terms of the configural learning theory of Pearce (1987,
1994), rather than in terms of the dynamics of Rescorla and Wagner’s
(1972) model.
The present study is a further investigation of whether superconditioning is in fact an empirical reality. Autoshaping rather than conditioned suppression was used as the method of Pavlovian conditioning.
We also used a within-subjects design rather than a between-groups
design in order to maximize sensitivity for detecting superconditioning. After initial training to peck the key light S1 when its presentation
was reinforced (S1), pigeons learned a discrimination between S1
versus the unreinforced presentation S1 in combination with a distinct
houselight, (H1 → S1). Rate of conditioning to three new key lights,
S2, S3, and S4, was then assessed according to the design shown in
Table 1. The critical comparison, in Phase 4, was the degree of conditioning to S2 versus S3 versus S4. If superconditioning does in fact
occur, conditioning should be greater to S3 than to the other two stimuli. S2 is the control for the rate of conditioning for a stimulus pre-
Table 1. Experimental design
Phase 2
Phase 3
Phase 4 test
S1 (4)
(H1 → S1) (12)
S1 (4)
(H1 → S1) (16)
S2/ (8)
(H1 → S3)/ (8)
(H2 → S4)/ (8)
S1 (4)
(H1 → S1) (16)
S2 (8)
S3 (8)
S4 (8)
Note. S1, S2, S3, and S4 were key lights; H1 and H2 were colored
houselights. Reinforced trials are indicated by , nonreinforced trials
by , and trials reinforced 50% of the time by /. The number of
trials per session is shown in parentheses for each trial type. Phase 1
consisted of autoshaping training with S1.
VOL. 13, NO. 5, SEPTEMBER 2002
sented alone, which is the control condition advocated by Navarro et
al. (1989). S4 provides the control for the rate of conditioning for a
key light preceded by a houselight without prior training as a conditioned inhibitor (H2), which is the control that has been used in other
studies of superconditioning.
METHOD
Subjects
Eight experimentally naive White Carneau pigeons served as subjects. They were maintained at approximately 85% of their free-feeding body weights by postsession feedings when necessary. The birds
were housed in individual cages under a 12-hr light/dark cycle, with
water and grit freely available.
Apparatus
Four operant chambers approximately 36 cm wide, 32 cm long,
and 35 cm high were used. Three translucent response keys that were
2.5 cm in diameter were mounted on the front intelligence panel 26
cm above the floor and 7.25 cm apart. Each key required a force of approximately 0.15 N to operate, and could be illuminated from the rear
by standard IEE 28-V 12-stimulus projectors that produced specific
forms on the key. Three 28-V, 1-W miniature lamps, one located 8.75
cm above each response key, served as houselights providing general
illumination. The left lamp was covered with a red cap, the middle
lamp was covered by a white cap, and the right lamp was covered with
a blue cap. Directly below the center key and 9.5 cm above the floor
was an opening 5.7 cm high by 5 cm wide that provided access to a solenoid-operated grain hopper. When activated, the hopper was illuminated from above with white light from a 28-V, 1-W miniature lamp.
A speaker mounted above the center of the ceiling provided continuous white noise throughout the experimental sessions. Experimental
events were controlled by IBM-compatible computers and a custombuilt interface.
Procedure
Stimuli
Four different key lights and two different houselights (in addition
to the main white houselight, which was extinguished when either the
red or the blue houselight was illuminated) were used to cue the various experimental conditions. Each key light was presented equally often on the left and right response keys. S1 was always a diffuse white
key light. S2, S3, and S4 were forms (triangle, circle, X, or vertical
line). The assignment of the specific forms to the different training
contingencies was randomized across subjects with the restriction that
each form stimulus was used for each stimulus contingency for 2 subjects. H1 and H2 were the red and blue houselights, counterbalanced
across subjects.
Training sequence
Table 1 shows the stimulus conditions during the different phases
of the experiment. Reinforced trials were followed by 3-s access to
grain. Each stimulus was presented for 6 s, and the intertrial interval
(ITI) was determined by a variable-time 90-s schedule. Compound
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Superconditioning
stimuli were presented sequentially: The houselight of a compound
was presented first for 6 s, and then the key light was presented for 6 s.
In Phase 1 (not shown in the table), all subjects were trained to respond to the S1 key light using an autoshaping procedure in which
food was delivered automatically at the end of the stimulus regardless
of whether the subject responded. Discrimination training between
S1 and (H1 → S1) was presented for 40 sessions in Phase 2. Additional trials involving S2, S3, and S4 were then added during Phase 3,
which continued for 10 sessions. For trials in which the new key lights
(S2, S3, and S4) were presented, food was presented on a 50% schedule. Finally, Phase 4 presented test trials in which S2, S3, and S4 were
presented alone with extinction in effect. During Phase 4, the discrimination between S1 versus (H1 → S1) continued to be maintained.
Phase 4 included two separate test sessions, separated by four sessions
of retraining with the conditions of Phase 3.
RESULTS AND DISCUSSION
Figure 1 shows the discrimination performance across the 40 sessions of discrimination training, in which the key light S1 was interspersed with the (H1 → S1) compound stimulus that served as the S.
Most subjects gradually learned not to peck on extinction trials when
S1 was preceded by H1. However, 2 subjects (331 and 290) responded
with consistently higher rates on S trials than on S trials for unknown reasons. For a 3rd subject (296), the response rate on S trials
was initially consistently higher than the response rate on S trials,
but the discrimination deteriorated during the last two blocks of training. It should be noted that autoshaping entails no response contingency in order for the food to be obtained, and that goal tracking
(approaching the food magazine) rather than key pecking occasionally
develops during autoshaping procedures. The 3 subjects for which the
discrimination ratio was not consistently high were removed from the
experiment at the end of Phase 2.
All 5 remaining subjects maintained a high level of discrimination
throughout Phase 3 training. Thus, the addition of the three new trial
Fig. 1. Discrimination performance across the 40 sessions of Phase 2
discrimination training. The graph shows results for individual subjects, as well as the mean across subjects.
456
types did not disrupt their performance. Figure 2 shows the average
number of responses per session to the key-light stimuli added in
Phase 3 (both in Phase 3 and in the retraining sessions of Phase 4). S3,
which was preceded by the conditioned inhibitor, H1, received the
highest mean number of responses (see the lower right-hand panel).
The mean numbers of responses to S2 and S4 were approximately
equal, but there was some variability across subjects. Bird 293 responded more to S2 than to S3, although responding to S3 was greater
than responding to S2 for the remaining 4 subjects. The results shown
in Figure 2 were analyzed with a two-factor (stimulus, block) repeated
measures analysis of variance, which included the data from the 10
sessions of Phase 3 and the 4 retraining sessions in Phase 4. The effect
of block was significant, F(6, 32) 24.7, p .01; the main effect of
stimulus was not significant, F(2, 8) 3.96, .10 p .05; the interaction was also not significant, F(12, 48) 1.2.
The critical data come from the test sessions during Phase 4. Two
separate test sessions were conducted, separated by retraining on the
Phase 3 contingencies. During these test sessions, all of the test stimuli were presented without being preceded by a houselight signal.
Note that this procedure is biased against demonstrating superconditioning if generalization decrement occurs, because S3 loses its preceding stimulus but S2 trials are unaffected. For the same reason, any
generalization decrement should be greater for S4 than for S2. Figure
3 shows the data separately for the two test sessions. Because the
mean data were similar for the two tests, the results of the tests were
combined for statistical analysis. Mean response totals across tests
were 158, 176, and 141, for S2, S3, and S4, respectively. All 5 subjects
responded more to S3 than to either S2 or S4. Four of 5 subjects responded more to S2 than to S4. Analysis of variance showed the effect
of the stimulus to be significant, F(2, 8) 9.4, p .01. Differences
between pairs of stimuli were analyzed with correlated t tests. Responses to S3 differed significantly from both responses to S2, t(4) 3.22, p .05, and responses to S4, t(4) 3.08, p .05, but responses
to S2 and S4 were not significantly different, t(4) 1.83, p .10.
Three subjects were eliminated from the experiment after training
in Phase 2 because they failed to attain the discrimination criterion.
This prevented the counterbalancing of stimuli that was part of the
original experimental design, thus raising the possibility that the results shown in Figure 3 reflect some type of stimulus bias. However,
an examination of the stimulus assignments for the 5 remaining subjects shows this not to be the case. Each of the four form stimuli was
used for at least 1 subject for each stimulus contingency, and no form
stimulus was used for more than 2 subjects for each stimulus contingency. Moreover, response rates averaged over the two critical test
sessions were highest for S3 for all 5 subjects even though only 2 subjects had the same form stimulus assigned to that stimulus contingency.
The relatively small differences in responses in the test sessions
suggest that superconditioning may be a relatively weak effect. However, the absolute size of the effect was perhaps reduced by stimulus
generalization among the different key-light stimuli. Because all of the
key lights were associated at least part of the time with food, there was
little reason for them to become sharply discriminated. Modifying the
procedure by including an additional key light that never is followed
by food should sharpen stimulus control by the different form stimuli
and therefore amplify the size of the superconditioning effect.
There are several possible reasons why the present study demonstrated superconditioning relative to both of the control conditions that
have been used in previous studies, whereas Navarro et al. (1989)
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Ben A. Williams and Margaret A. McDevitt
Fig. 2. Average number of responses per session to the novel key-light stimuli that were added during Phase 3. Also
shown is the average number of responses to the same stimuli during the retraining sessions of Phase 4. Data are combined
for two-session blocks. Results for individual subjects and the means across subjects are graphed separately.
demonstrated it only with respect to the control condition in which the
novel CS was paired with an untrained novel stimulus. The most obvious explanation is the difference in conditioning preparation: autoshaping with pigeons versus conditioned suppression with rats. But
a more likely explanation, in our view, is that the present procedure
was probably more effective in maintaining conditioned inhibition
while the novel CSs were being trained in Phase 3. It is also possible
VOL. 13, NO. 5, SEPTEMBER 2002
that our use of a within-subjects design provided a more sensitive test
than the between-subjects experimental designs used in other experiments.
The theoretical interpretation most consistent with the present findings is that a stimulus trained as a conditioned inhibitor generates a
negative expectation about US occurrence. Accordingly, when the US
does occur, it is less expected than if the stimulus were associatively
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Superconditioning
Fig. 3. Number of responses to the novel key-light stimuli in Phase 4.
The top and bottom panels show the results from the first and second
test sessions, respectively. During these sessions, all of the test stimuli
were presented without a preceding houselight; the original discrimination was maintained. Results for individual subjects and the mean
across subjects are shown.
neutral, and greater learning is the result. The empirical reality of superconditioning thus provides prima facie evidence that inhibitory associations do in fact occur.
A possible alternative explanation of our results is that provided by
Pearce and Redhead (1995) for their own demonstration of superconditioning. They presented conditioning to AX and B after prior
training with A, AX, and B versus prior training with A, X,
and B. In subsequent testing, conditioning was greater to A than to
B in the former case but not in the latter. Thus, their results are similar
to our own in showing enhanced conditioning to a novel CS in the
presence of a conditioned inhibitor. However, they interpreted their
results in terms of Pearce’s (1987, 1994) configural theory of discrimination. That account depends critically on stimulus generalization be-
458
tween the stimulus compound AX and A, which augments the associative strength derived from A’s own pairings with the US.
Such an account cannot be applied easily to the present results. According to that view, responding to S3 during the test trials would be the
result of a two-step generalization of inhibition of the compound (H1 →
S1) to S3. That is, the inhibition trained to (H1 → S1) would generalize to (H1 → S3). Then, because of that generalized inhibition, additional excitatory conditioning would occur in response to the latter
compound until the sum of the generalized inhibition and the excitation
due to the (H1 → S3) pairings reached asymptote. But response to S3
alone would then be some fraction of that asymptotic level, depending
on the degree of generalization from the (H1 → S3) compound to S3
alone. Given that the same asymptotic level was established for S2 directly, there appears to be no way that Pearce’s configural theory could
explain the superconditioning to S3 that was observed.
Also consistent with the generality of superconditioning are the results of experiments in which stimuli previously paired with food are
paired with shock in compound with a second stimulus not previously
trained. For example, Dickinson (1977) reported greater fear conditioning to a CS paired with shock if it was presented with a second
stimulus previously paired with food than if the CS alone was paired
with shock. This superconditioning occurred because the CS for
food signaled a positive US, and thus there was a discrepancy between
the expected and actual outcome, whereas when the CS was presented
alone there was no particular outcome expected. Analogously, Fowler,
Fago, Domber, and Hochhauser (1973) demonstrated that a CS for
shock enhanced appetitive learning of a maze discrimination when the
CS accompanied food in the goal box; in addition, the presentation
in the goal box of a CS for shock retarded the acquisition of the discrimination. Such results suggest that conditioned inhibitors for aversive USs are functionally equivalent to conditioned excitors for appetitive
USs, and vice versa. Such functional equivalence could occur only if
conditioned inhibitors produce negative expectations about the US occurrence.
The equivalence of a CS for shock with an appetitive CS is, of
course, the cardinal assumption of the safety-signal theory of avoidance learning, which provides a persuasive account of much of the extant data in that area of research (see Dinsmoor, 2001, for a recent
review). That a CS for shock can serve as an effective positive conditioned reinforcer for bar pressing in rats has been empirically demonstrated by Rescorla (1969). The relevance of such results to the
present study is that such transfer between aversive and appetitive
training procedures relies critically on the concept of conditioned inhibition producing a negative expectation with respect to the occurrence
of a US. The present demonstration of superconditioning provides further support for that view.
Finally, the present results have implications for rule-based accounts of conditioning, which entail that superconditioning should not
occur (Holyoak, Koh, & Nisbett, 1989). Given the empirical reality of
superconditioning, such theories must be modified or rejected.
Acknowledgments—This research was supported by National Institute of
Mental Health Grant MH 57334.
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