On the differences in degree of renewal produced by the different renewal designs

Highlights

• Differences in degree of recovery from extinction among the different renewal designs arise from multiple factors.

• The excitatory training context can play a role in renewal both as a summative excitor when testing occurs in the training context and as a comparator stimulus.

• Renewal effects are determined by a number of contributing mechanisms.

Abstract

This paper addresses sources contributing to the differences in the degree of recovery from extinction observed with different renewal paradigms. In two lick suppression experiments with rats, we assessed the role of the associative status of the acquisition context in both the weakness of AAC renewal and the sometimes observed weaker renewal resulting from an ABC design relative to an ABA design. In Experiment 1, we observed that AAC renewal relative to an AAA control group was small unless Context A had undergone associative deflation (i.e., extinction of Context A). Deflation of Context A not only decreased behavioral control by the CS in the AAA condition, but increased it in the AAC condition, thereby implicating a comparator process in addition to associative summation between the CS and test context. In Experiment 2, an excitatory acquisition context was found to enhance the difference between ABC and ABA renewal. Associative deflation of the acquisition context decreased ABA renewal more than ABC renewal. Thus, the associative value of the acquisition context (A) was more positively related to the level of renewal when the target CS (X) was tested in this context than when it was tested in a neutral but equally familiar context (C), consistent with the frequently observed greater renewal in an ABA condition than an ABC condition arising from associative summation of the CS and test context. These findings demonstrate that the excitatory status of the acquisition context influences the observed degree of renewal.

Introduction

Renewal can be behaviorally defined as the recovery of an extinguished response when testing occurs in a context different from that in which the extinction treatment took place. This behavioral definition is not to be confused with one that is based on a specific underlying mechanism. There are a number of different procedures to implement a context shift between extinction and testing. A classic example is a preparation in which acquisition, extinction, and testing each occur in separate contexts (i.e., ABC renewal, wherein the first letter denotes the acquisition context, the second letter denotes the extinction context, and the third letter denotes the test context; e.g., Bouton and Bolles, 1979). Additionally, robust renewal has been observed when acquisition and testing occur in the same context, but extinction occurs in a second context (i.e., ABA renewal; e.g., Bouton and King, 1983). Although ABC and ABA renewal often produce similar levels of recovery, ABC renewal tends to result in a nominally weaker conditioned response (e.g., Thomas et al., 2003). Finally, renewal can sometimes be observed when acquisition and extinction take place in the same context, and testing occurs in a different context (i.e., AAC renewal; e.g., Bouton and Ricker, 1994).

Although each of these paradigms can produce behavioral renewal, it is generally accepted that the magnitude of recovery varies across the different renewal designs. The AAC (also referred to as AAB) renewal paradigm has been shown to produce the weakest amount of recovery from extinction when compared to either ABC or ABA renewal, and sometimes recovery may not be observed at all (e.g., Laborda et al., 2011b, Tamai and Nakajima, 2000, Tamai et al., 2001, Thomas et al., 2003). Interpretation of a comparison between AAC renewal and either ABC or ABA renewal is complicated because AAC renewal does not involve a context shift between acquisition and extinction, whereas ABC and ABA renewal do. A direct comparison between ABC and ABA renewal is simpler to interpret as the two designs differ only in the change in context at the time of testing. This can also be seen in the fact that both ABA and ABC designs ordinarily make use of the same control condition (i.e., ABB), whereas AAC renewal usually employs a different control condition (i.e., AAA).

Several accounts of renewal have been suggested based on the view that the test context modulates retrieval of the memory produced by extinction (e.g., Bouton, 1993, Miller and Escobar, 2002, Rosas et al., 2006). Bouton proposed that extinction treatment produces an inhibitory association between the conditioned stimulus (CS) and the unconditioned stimulus (US). This inhibitory association is assumed to be more context specific than the excitatory CS-US association (either because it is inhibitory or because it is second learned; e.g., Bouton, 1993, Bouton, 1997, Nelson, 2002). This context specificity of inhibitory associations results in behavior indicative of excitation when testing occurs outside the context of extinction treatment. In this framework, the extinction context serves as a negative occasion setter (Holland, 1989) that modulates the expression of the inhibitory relationship. Miller and Escobar's and Rosas et al.’ accounts of renewal are variants of Bouton's explanation, but make the same predictions with respect to the present research. Hence, we will not speak further to Miller and Escobar's and Rosas et al.’s accounts here. Critically, Bouton's account by itself, although well able to explain the basic renewal effect, seemingly incorrectly anticipates equal degrees of renewal across the three types of renewal designs. However, one might argue that learning that the extinction context is a negative occasion setter should be less effective in an AAC design than an ABC or ABA design because in the AAC design the extinction context was also the acquisition context, making the extinction context a less effective discriminative stimulus. Thus, Bouton's account, with this minor added feature, may be viewed as anticipating AAC renewal to be weaker than the other two renewal designs. But there is nothing in Bouton's account to explain why ABC renewal is often somewhat weaker than ABA renewal.

The most frequently cited alternative to Bouton's (1993) account of renewal is based on the view that renewal is the result of direct associations between the various contexts and US. One potential example of this sort of association is that the extinction context could become inhibitory due to presentations of the excitatory CS occurring within it in the absence of the US (i.e., in an ABB control condition; see Polack et al., 2012, for supporting data). This inhibitory potential of the extinction context could both protect the CS from unlearning of the CS-US association during extinction treatment (McConnell and Miller, 2010, Rescorla, 2003) and reduce responding to the CS during a test of the CS in the extinction context, as in an ABB control group. If the extinction context functions as a conditioned inhibitor during testing in the extinction context, then responding to the target CS would be expected to recover outside of the extinction context. Thus, this account is able to explain the basic renewal effect. Granted there are many demonstrations of failures to observe any inhibitory status of the context, suggesting that direct inhibition of the US by the extinction context is at most only one of the several sources of renewal (Bouton and King, 1983, Bouton and Swartzentruber, 1986, Nelson et al., 2011, Rescorla, 2008). However, this rejection of the view that the extinction context becomes inhibitory is, by its nature, predicated on null results. Additionally, there is a bias in the renewal literature toward using parameters that encourage contextual modulation of memories of extinction, rather than those parameters that encourage modulation of responding to the target cue by an inhibitory extinction context (in contrast, Polack et al. used parameters biased to enhance the inhibitory value of the extinction context). Accounts of renewal that focus on the associative status of the test context not only emphasize the possibility that the extinction context is inhibitory, but that the acquisition context may be excitatory. An excitatory acquisition context could result in associative summation of the CS and the test context if testing occurs in the acquisition context, as in an ABA renewal condition. This sort of associative summation could explain part or all of ABA renewal and is at least a plausible contender in explaining why ABA renewal is often more robust than ABC renewal, in which testing occurs in a neutral context. Moreover, due to Context A's initial potential for excitatory value from CS-US acquisition occurring in Context A, Context A may be slow to acquire inhibitory value during extinction when extinction occurs in the acquisition context. This could result in low contextual inhibition of responding to the CS when the CS is tested in the acquisition context (i.e., an AAA condition). The resultant heightened (i.e., uninhibited) responding to the CS in Context A would diminish the difference between an AAC renewal condition and its AAA control. Thus, consideration of the associative status of the extinction and test contexts provide a potential account not only of the basic renewal effect, but the observed differences in degree of recovery among the three types of renewal designs (i.e., AAC < ABC ≤ ABA). However, accounts of renewal based on associative summation with the extinction and/or test contexts are challenged by considerable evidence that renewal can occur even when the associative status of the contexts in the renewal and control conditions have been equated (e.g., Harris et al., 2000). Thus, accounts based on potential differences in the associative status of the contexts alone are not able to account for all reports of renewal.

In addition to these two families of mechanisms that may contribute to renewal effects, there are other models (e.g., Larrauri and Schmajuk, 2008). But these models tend to invoke a large number of independent mechanisms (and hence a large number of free parameters) that preclude their making unambiguous a priori predictions although they can often be made to fit the data post hoc. Hence, we will not pursue such models here.

Although the basic renewal effect can be interpreted in terms of either modulation of responding to the target by the test context or the associative status of the test context, neither account is fully adequate. ABA renewal being more robust than ABC renewal challenges the completeness of the contextual modulation account, and evidence of renewal even when the associative histories of the different contexts have been equated challenges the completeness of accounts dependent on the associative status of the contexts. However, these two roles of the context are not mutually exclusive. Holland (1985) and others have established that an occasion setter can simultaneously be a Pavlovian CS. The intent of the present research was to examine the contribution of associations between the test context and the US in producing the differences observed in the magnitude of the different types of renewal.

The question addressed in Experiment 1 was whether the acquisition context-US association contributes to the frequently observed weakness of AAC renewal. During acquisition (i.e., CS-US pairings), the acquisition context (i.e., A) presumably enters into an excitatory association with the US which may then summate with the residual excitatory strength of the extinguished stimulus when testing occurs in that context, as in the AAA control condition to which AAC renewal is ordinarily compared. Thus, responding at test in the AAA control condition may reflect not just responding to the extinguished CS, but responding to the conjoint stimulus and the excitatory context. This increased responding in the AAA control group due to associative summation could reduce the difference in responding between recovery from extinction in an AAC renewal group and its AAA control group. Several renewal demonstrations have directly assessed the associative value of the acquisition context and found that this context alone did not elicit a conditioned response (e.g., Bouton and King, 1983); however, the context used by Bouton and King may have had a low associative strength that was merely below the threshold required to observe a conditioned response. Any subthreshold response potential of the context could still be available to summate with the residual response potential of the extinguished CS (see Reberg, 1972). A similar account may be proffered for the comparison between ABC and ABA renewal effects to explain why ABA renewal is often slightly more robust than ABC renewal. That is, at test for an ABA group the associative strength of the test context (A) could summate with the residual associative strength of the target CS, whereas for an ABC group an excitatory context is absent during CS testing. In Experiment 2, we examined this possibility. Several clever designs have attempted to completely rule out the potential contribution of direct context associations by perfectly matching experience between test contexts in order to highlight the contribution to renewal of occasion setting by the extinction context (e.g., Harris et al., 2000, Rescorla, 2008). Renewal seen in these studies makes clear that associations of the US to the test context are not adequate to account for all instances of renewal. Although controlling for associative experience between test contexts is an excellent strategy for studying the potential occasion setting properties of the extinction context, such designs eliminate other potential contributing mechanisms that may be involved in settings that are more ecologically valid in modeling relapse from exposure therapy (e.g., Laborda et al., 2011a). The present manuscript serves to highlight the relevance of some additional contributing mechanisms; however, we are not prepared to suggest that the present parameters have more clinical relevance than others. The potential contribution of various renewal mechanisms would depend on the nature of acquisition, treatment, and testing conditions specific to an individual patient, the etiology of the disorder, and the particular clinical setting.