Behavioral Inhibition

Behavioral inhibition is a consequence of an animal's capacity to learn both positive and negative relationships, whether these relationships involve stimuli or responses. The term arises from the seminal work of Pavlov (1927) in his studies of conditioned reflexes in hungry dogs. Pavlov found that an initially neutral conditioned stimulus (CS), such as the sound of a metronome, could acquire significance if it predicted the delivery of an unconditioned stimulus (US), such as meat powder. After a number of CS-US pairings, the CS would come to evoke a conditioned response (CR), such as salivation. This form of behavioral adaptation, known as excitatory conditioning, allowed the animal to prepare for the arrival of the US. Inhibitory conditioning is the counterpart of excitatory conditioning. Pavlov found that an initially neutral CS would acquire the ability to suppress the salivary CR (behavioral inhibition) if the CS signaled the absence of an expected US.

In Conditioned Reflexes (1927), Pavlov listed four experimental conditions under which responding is inhibited: (1) suppression of the CR evoked by an excitatory CS in the presence of a second "inhibitory" CS, (2) the gradual loss of the CR in extinction, (3) decreased generalized responding to an unreinforced CS when trained concurrently with a reinforced CS (called differential conditioning), and (4) diminution of the CR in the early portion of a long-duration CS. The first procedure is now the paradigmatic instance of what is called inhibitory conditioning.

Although Pavlov emphasized the importance of inhibitory conditioning, the idea was not initially well received. Interest in inhibitory conditioning was reawakened with the incorporation of inhibitory conditioning into correlative accounts of conditioning (e.g., Rescorla, 1967). During this time, the concept of inhibition also proved to be a powerful vehicle for understanding a wide range of clinically relevant behavioral phenomena. Of special interest was the persistence of phobic avoidance in the absence of further traumatic events. But the key development was Rescorla's (1969) introduction of the summation and retar dation tests. These special tests could be applied to detect the presence of inhibition independently of the conditions under which it was observed.

Since its first introduction, the idea that a CS may possess inhibitory properties has stirred a great deal of controversy. How can a CS be declared inhibitory merely on the basis of a reduction in the probability of the CR? To resolve such a controversy, it is necessary to exclude alternative accounts. Historically, three general types of alternatives have been offered. One invokes competition between incompatible reactions. The second possibility is that an inhibitory CS draws attention away from other excitatory stimuli and is merely an attentional distractor. The third is that reduced responding is not a matter of inhibition but rather of less excitation.

Rescorla (1969) argued that an inhibitory CS should acquire properties opposite to those of an excitatory CS, if inhibition involved learning that a CS and US were negatively correlated. One test designed to show the opposi-tional properties of an inhibitory CS was called summation. If a CS were truly inhibitory, it should reduce the probability that an excitatory CS would evoke its usual CR when the two stimuli were presented in compound for the first time. To rule out attentional distraction, the reductions obtained should be greater than those produced by a control CS that was uncorrelated with the US. Further evidence of inhibition would be shown by retardation of acquisition in which the inhibitory CS is transformed into an excitatory CS. The required finding is that conditioning should proceed more slowly than transformation of a neutral CS into an excitor. These two tests, taken together, are still accepted by most in the field as firm evidence of inhibition.

Equipped with tests for verifying the status of an inhibitory CS, researchers turned to the question of the psychological basis for behavioral inhibition. On the basis of Pavlov's work, one might speculate that an inhibitory CS signals a period during which the US is absent. This can be shown to be false. If two distinctive CSs are paired on separate trials with the same US, and both CSs together are then combined with a third CS and the triplet is reinforced, it turns out that the third CS acquires the properties of a conditioned inhibitor, even though it does not signal the absence of the US (Kremer, 1978). However, this procedure also suggests an answer. When two excitatory CSs are combined, unusually high levels of excitation are elicited— much higher than can be sustained by a single US. Hence, although the third CS does not predict the nonoccurrence of the US, it does predict that the single US received will be less than is predicted by the two excitatory CSs. Thus, conditioned inhibition seems to develop when the US received is less than that anticipated. This is currently the most accepted psychological account (Wagner & Rescorla, 1972).

Experimentation has also revealed that an extinguished CS does not actually lose its excitatory power as the term extinction suggests. Instead, the excitatory CS acquires a new inhibitory association that joins the already present excitatory association. That extinction does not erase the original excitatory association is abundantly clear if one reminds the animal of the earlier association. For example, if acquisition takes place in a different experimental context than extinction, a return to the context of acquisition causes renewal of the original CR (Bouton, 1993). Renewal is of obvious importance for our understanding and treatment of anxiety disorders. Conditioned fears are never truly lost (extinguished) but are only inhibited. It should be apparent from this last example that behavioral inhibition is a rich area for the application of basic research to psychological dysfunctions.

REFERENCES

Bouton, M. E. (1993). Context, time, and memory retrieval in interference paradigms in Pavlovian learning. Psychological Bulletin, 114, 80-99. Kremer, E. F. (1978). The Rescorla-Wagner model: Losses in associative strength in compound conditioned stimuli. Journal of Experimental Psychology: Animal Behavior Processes, 4, 22-36. Pavlov, I. P. (1927). Conditioned reflexes. Oxford, UK: Oxford University Press.

Rescorla, R. A. (1967). Pavlovian conditioning and its proper control procedures. Psychological Review, 74, 71-80. Rescorla, R. A. (1969). Pavlovian conditioned inhibition. Psychological Bulletin, 72, 77-94. Wagner, A. R., & Rescorla, R. A. (1972). Inhibition in Pavlovian conditioning: Application of a theory. In R. A. Boakes & M. S. Halliday (Eds.), Inhibition and learning. London: Academic Press.

Douglas A. Williams

University of Winnipeg, Winnipeg, Canada

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