One-trial backward excitatory fear conditioning in rats: Acquisition, retention, extinction, and spontaneous recovery

Abstract

Water-deprived male albino rats received a single presentation of a 4-sec electric-grid-shock unconditioned stimulus followed by a 4-sec white-noise conditioned stimulus (a single backward conditioning trial.) Excitation conditioned to the noise was indexed in terms of the noise's subsequent ability to suppress ongoing licking of a water tube. The main findings were: (1) Excitation was acquired and was retained over a 30-day retention interval; (2) although excitation was retained, it did not grow significantly stronger during the interval (there was no incubation effect); (3)excitation was extinguished by noise-alone trials; and (4)excitation showed more spontaneous recovery when extinction trials were separated by 29 days than when separated by only 1 day. Because these results are similar to those in the forward conditioning literature, they seem consistent with, but do not demand, the view that forward and backward excitatory conditioning involve similar learning processes. A current theory that embraces this view is opponent-process theory (Solomon & Corbit, 1974). We suggest that opponent-process theory can (1)account for existing backward conditioning data, (2) explain the phenomenon of incubation that has previously been described in the literature while simultaneously explaining its absence in the present study, and (3)integrate certain nonmonotonic acquisition phenomena that have appeared in both the forward and backward conditioning literatures.Reports that conditioned excitation can be established through backward conditioning procedures have for years met with skepticism (e.g., Kimble, 1961;Mackintosh, 1974;Osgood, 1953;Underwood, 1949). Indeed, backward conditioning procedures have often been used in classical conditioning experiments as control procedures designed to leave the conditioned stimulus (CS) neutral. Furthermore, when this practice was eventually criticized (Rescorla, 1967), the criticism was not that the CS might become excitatory but, rather, that it might acquire an opposite, inhibitory tendency. Such conditioned inhibition is clearly predicted by several modern theories of conditioning, including contingency theory (Rescorla, 1967) and discrepancy theory (Rescorla & Wagner, 1972). More generally, conditioned inhibition is predicted by any theory that emphasizes the information that CSs provide about unconditioned stimuli (USs). Since backward CSs usually predict relatively long periods of US absence (e.g., Moscovitch & LoLordo, 1968), they are expected to acquire conditioned properties opposite to those of CSs that predict the imminent occurrence of USs. Empirical support for this predicted conditioned inhibition has been accumulating in recent years and now appears substantial (Heth, 1976;Maier, Rapaport, & Wheatley, 1976;Moscovitch & LoLordo, 1968;Plotkin & Oakley, 1975;Siegel & Domjan, 1971, 1974. In addition, it has also been shown that backward (US-CS) pairings can serve to extinguish excitatory conditioning based on forward (CS-US) pairings (Ayres, Mahoney, Proulx, & Benedict,...

One-trial backward excitatory fear conditioning transfers across contexts

“…Perhaps if the differences between them were enhanced, backward excitatory fear conditioning would not survive. Second, although we have found statistically significant evidence for one-trial backward excitatory fear conditioning both here and in several other reports from this laboratory (Albert, 1990;Ayres et al, 1987;Mahoney & Ayres, 1976;Shurtleff & Ayres, 1981;van Willigen et al, 1987), none of those effects has been large. It is yet unclear whether these small effects simply reflect our ignorance about appropriate conditioning parameters or whether these effects are as large as they get.…”

“…According to these writers, there is little evidence in the experimental literature for one-trial Pavlovian fear conditioning. In contrast to Sturgis and Scott, we believe that there are numerous examples of one-trial fear conditioning in the animal experimental literature, including several reports from our own laboratory (Albert, 1990;Ayres, Haddad & Albert, 1987;Burkhardt & Ayres, 1978;Mahoney & Ayres, 1976;Shurtleff & Ayres, 1981;van Willigen, Emmett, Cote & Ayres, 1987). The present results will add to that body of data.…”

“…Even so, evidence is mounting that backward fear conditioning procedures using a small number of trials can indeed establish measurable conditioned fear to the backward-paired CS (for a review, see Spetch, Wilkie & Pinel, 1981). Again, the demonstrations from our own laboratory seem especially relevant because they were based on only a single backward conditioning trial (Albert, 1990;Ayres et al, 1987;Mahoney & Ayres, 1976;Shurtleff & Ayres, 1981;van Willigen et al, 1987).Moreover, in contrast to an earlier claim for one-trial backward excitatory fear conditioning (Keith-Lucas & Guttman, 1975), these studies used white noise or tone as CSs, stimuli that are thought to have no particular biological relevance to the rat Ss.One undesirable aspect of the existing evidence for one-trial backward excitatory fear conditioning, however, is that every demonstration so far has involved testing for conditioning to the CS in the same context in which the conditioning took place. Clearly, human phobias transfer readily across contexts.…”

“…Even so, evidence is mounting that backward fear conditioning procedures using a small number of trials can indeed establish measurable conditioned fear to the backward-paired CS (for a review, see Spetch, Wilkie & Pinel, 1981). Again, the demonstrations from our own laboratory seem especially relevant because they were based on only a single backward conditioning trial (Albert, 1990;Ayres et al, 1987;Mahoney & Ayres, 1976;Shurtleff & Ayres, 1981;van Willigen et al, 1987).…”

CS modality effects in one-trial backward and forward excitatory conditioning as assessed by conditioned suppression of licking in rats

“…In contrast, successful demonstrations of conditioning to white noise and tone CSs are common, even with only one conditioning trial and regardless of whether the CS occurs before, during, or after the US (Burkhardt, 1980;Burkhardt & Ayres, 1978;Mahoney & Ayres, 1976;Shurtleff & Ayres, 1981). The present paper provides some clues as to why the light may be seldom used in the lick-suppression literature.…”