Secondary extinction in Pavlovian fear conditioning

Pavlov (1927/1960) reported that following the conditioning of several stimuli, extinction of one conditioned stimulus (CS) attenuated responding to others that had not undergone direct extinction. However, this secondary extinction effect has not been widely replicated in the contemporary literature. In three conditioned suppression experiments with rats, we further explored the phenomenon. In Experiment 1, we asked whether secondary extinction is more likely to occur with target CSs that have themselves undergone some prior extinction. A robust secondary extinction effect was obtained with a nonextinguished target CS. Experiment 2 showed that extinction of one CS was sufficient to reduce renewal of a second CS when it was tested in a neutral (nonextinction) context. In Experiment 3, secondary extinction was observed in groups that initially received intermixed conditioning trials with the target and nontarget CSs, but not in groups that received conditioning of the two CSs in separate sessions. The results are consistent with the hypothesis that CSs must be associated with a common temporal context during conditioning for secondary extinction to occur.     

Second-order conditioning detects unexpressed morphine-induced salt aversion

Morphine failed to condition a salt taste aversion at a dose (15 mg/kg) sufficient to produce a robust aversion to a saccharin taste. Indeed, three different concentrations of salt (1%, 1.5%, and 2%) paired with the same morphine dose yielded no direct evidence for conditioned aversion. Yet, when a novel saccharin taste was paired in compound with the previously conditioned salt conditioned stimulus, we found evidence for a conditioning to the saccharin cue alone in three separate experiments. Control groups eliminated alternative accounts such as neophobia and differential exposure to morphine. Combined, these findings indicate that morphine conditioned a salt aversion. Although this aversion was not directly expressed, a second-order conditioning procedure was able to provide a more sensitive index of conditioning.     

Trace and long-delay fear conditioning in the developing rat

In two experiments with rats, we examined the developmental emergence of conditioned freezing following trace and short-delay conditioning and also included a long-delay comparison group. In the short-delay and trace groups, a 10-sec conditioned stimulus (CS) was paired with shock; for the trace rats, a 10-sec trace interval followed CS termination. The long-delay groups received a 20-sec CS paired with shock, to equate for the longer interstimulus interval (ISI) in the trace group. Trace conditioning emerged later in development than did short-delay conditioning (see Moye & Rudy, 1987). Importantly, long-delay conditioning emerged in parallel with trace conditioning, at a similar time, and with similar strength. These findings suggest a role for the longer ISI, as opposed to the unfilled gap per se, in the late emergence of trace conditioning. The role of the hippocampus in trace conditioning and the possibility that young rats encode the temporal relationship between CSs and unconditioned stimuli are also considered.     

US inflation with trace and simultaneous fear conditioning

Two experiments with rat subjects in a conditioned punishment paradigm are reported. These experiments attempted to determine if the events entering into association with the CS following conditioning with informative (forward) and noninformative (simultaneous) CSs were comparable. In Experiment 1, exposure to intense shock alone following trace (ISI = 10 sec) conditioning with moderate shock enhanced the suppressive effects of a 2-sec CS. A similar manipulation following explicitly unpaired CS-US presentations (ISI = 2 min) had no effect. These data were taken as evidence that the CS and US were associated during trace conditioning. Experiment 2 showed that exposure to intense shock following simultaneous conditioning also enhanced suppression to the CS. These results suggested that simultaneous and forward conditioning procedures yield similar forms of associative learning.     

Reward devaluation disrupts latent inhibition in fear conditioning

Three experiments explored the link between reward shifts and latent inhibition (LI). Using consummatory procedures, rewards were either downshifted from 32% to 4% sucrose (Experiments 1–2), or upshifted from 4% to 32% sucrose (Experiment 3). In both cases, appropriate unshifted controls were also included. LI was implemented in terms of fear conditioning involving a single tone-shock pairing after extensive tone-only preexposure. Nonpreexposed controls were also included. Experiment 1 demonstrated a typical LI effect (i.e., disruption of fear conditioning after preexposure to the tone) in animals previously exposed only to 4% sucrose. However, the LI effect was eliminated by preexposure to a 32%-to-4% sucrose devaluation. Experiment 2 replicated this effect when the LI protocol was administered immediately after the reward devaluation event. However, LI was restored when preexposure was administered after a 60-min retention interval. Finally, Experiment 3 showed that a reward upshift did not affect LI. These results point to a significant role of negative emotion related to reward devaluation in the enhancement of stimulus processing despite extensive nonreinforced preexposure experience.     

Second-order conditioning of the conditioned emotional response: Some methodological considerations

Employing rats in a CER procedure, the present study sought to determine the extent to which the second-order conditioning effects reported by Rizley and Rescorla (1972) represented first-rather than second-order conditioning. Subjects receiving first-order pairings of flashing light (CS₁) and shock followed by second-order pairings of noise (CS₂) and CS₁ displayed greater suppression to CS₂ than did control subjects receiving second-order pairings in the absence of first-order conditioning. This was true whether or not control subjects had experienced unsignaled shock or habituation to CS₁ prior to CS₂CS₁ pairings. Simple stimulus pairings did produce some suppression to CS₂, however. The procedure developed by Rizley and Rescorla (1972) appears to be a reliable means for producing and studying second-order aversive conditioning.     

Second-order conditioning of the pigeon’s keypeck

Pigeons learned to peck a keylight (S2) when it was paired with a stimulus (S1) that already evoked keypecking. Control procedures showed that S2 acquired control over responding because it was paired with S1 and because S1 had a conditioning history, thereby supporting the claim that S2 was a second-order conditioned stimulus. Second-order conditioning occurred as rapidly when S1 was a keylight as when it was a tone. Test procedures showed that after second-order conditioning, responding to S2 was markedly debilitated by the extinction of responding to S1, indicating that the ability of S2 to evoke a response importantly depends upon the continued ability of S1 to do so. Our demonstration that directed motor action in the pigeon is susceptible to second-order conditioning suggests a new interpretation of conditioned reinforcement in instrumental learning. Our demonstration that the effectiveness of S2 depends upon the continued effectiveness of S1 indicates that S-S associations are formed in this version of the second-order conditioning experiment.     

Second-order conditioning: The importance of stimulus overlap on second-order trials

Second-order conditioning was examined using the rabbit eyeblink paradigm and the gerbil CER paradigm. Pavlov’s hypothesis that stimulus overlap on second-order trials produces conditioned inhibition and that nonoverlap leads to second-order conditioning was not confirmed. Our results also revealed that the manner in which first-order and second-order trials are intermixed has an important influence on the properties of the second-order CS. A within-session mixture of first- and second-order trials tended to produce second-order conditioning, and a between-session mixture tended to produce conditioned inhibition. Second-order conditioning was more prominent with the gerbil fear response than with the rabbit eyelid response.     

Blocking and enhancement of fear conditioning by appetitive CSs

Prior research on Pavlovian-to-instrumental transfer has shown that when a CS previously associated with shock (AvCS+) is presented contingent upon a choice response to a discriminative stimulus for food reinforcement, it facilitates discrimination learning. Conversely, a response-contingent CS previously associated with the absence of shock (AvCS?) retards discrimination learning. To evaluate whether these findings reflect across-reinforcement blocking and enhancement effects, two experiments investigated the effects of appetitively conditioned stimuli on fear conditioning to a novel stimulus that was serially compounded with the appetitive CS during conditioned-emotional-response (CER) training. Although there were no differential effects of the appetitive CSs in CER acquisition, Experiment 1, using a relatively weak shock US, showed that a CS previously associated with food (ApCS+) retarded CER extinction to the novel stimulus, in evidence of enhanced fear conditioning to that stimulus. In addition, Experiment 2, using a stronger shock US, showed that a CS previously associated with the absence of food (ApCS?) facilitated CER extinction to the novel stimulus, in evidence of weaker fear conditioning to that stimulus. These results parallel traditional blocking effects and indicate not only that an ApCS+ and an ApCS? are functionally similar to AvCSs of opposite sign, but that their functional similarity is mediated by common central emotional states.     

Second-order conditioning using a contextual stimulus as S1

Three experiments investigated the question of whether a spatial stimulus, a context, could function as S₁ in a second-order conditioning procedure. In each experiment, rat subjects were presented with S₁-US pairings by being given footshocks in one of two contexts. Forty-eight hours later, the experimental groups received S₂-S₁ pairings, during which a tone was presented in the training context. As measured by a lick-suppression test administered in a third context, rats were more fearful of the tone if it occurred in the context in which they had previously been shocked. The training context in each experiment apparently served to establish second-order fear conditioning to the tone.     

Second-order sexual conditioning in male Japanese quail (Coturnix japonica)

Second-order conditioning of social approach to a female conspecific in male Japanese quail was investigated in four experiments. Subjects that received paired first- and second-order trials acquired second-order conditioning in both Experiments 1 and 2. In contrast, subjects that received paired first-order but unpaired second-order trials, and subjects that received unpaired first-order but paired second-order trials, did not acquire second-order conditioning. In Experiment 3, subjects for whom the first-order conditioned stimulus was presented in extinction showed second-order conditioning comparable to that shown by subjects in a control group that did not receive the extinction procedure. In Experiment 4, subjects approached a second-order stimulus less when sexually satiated than when sexually deprived. These findings suggest that second-order sexual conditioning in quail is mediated by an association of the second-order stimulus with a representation of the unconditioned stimulus.     

Blocking in eyelid conditioning: Effect of changing the CS-US interval and introducing an intertriai stimulus

Kamin’s three-stage blocking paradigm was investigated in rabbit eyelid conditioning, Two manipulations were examined. A change in the CS-US interval from Stage 1 to Stage 2 did not attenuate blocking. The introduction of a salient stimulus during the intertriai interval in Stage 2 also failed to attenuate blocking. The first result is not consistent with Kamin’s interpretation of the blocking effect in terms of US surprisingness. The second resuit is inconsistent with a prediction based on the Rescorla-Wagner model.     

One-trial context fear conditioning with immediate shock: The roles of transport and contextual cues

In three experiments, using a total of 120 albino rats, we assessed whether transportation cues might evoke some of the freezing (i.e., defensive immobility) that we see in a context on a day following a footshock given immediately after placement in that context. The results suggested that immediate shock could directly condition strong fear to both simulated and actual transport cues. Although conditioning to transport cues explains some of the freezing that is seen on the test day, it does not explain all of it. We also found evidence that some of the freezing is due to conditioning to permanent features of the context in which the immediate shock is given. The results support a role for transport cues in theories of context conditioning and argue against shock-processing accounts of the conditioning deficit that results from immediate shock.     

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

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.     

One-trial simultaneous and backward fear conditioning as reflected in conditioned suppression of licking in rats

In three experiments, groups of albino rats received one strictly simultaneous pairing of a 4-sec auditory conditioned stimulus (CS) and a 4-sec 1-mA shock unconditioned stimulus (US). Other groups received a backward pairing, in which the US began before the CS, or a forward pairing, in which the CS began before the US. Control groups received only the US or received both the CS and the US but widely separated in time. Later, the CS was presented while the rats licked a drinking tube for water, and CS-elicited suppression of licking was taken as an index of the Pavlovian conditioned response (CR). It was found that groups receiving a single forward or a single simultaneous pairing suppressed more than groups that had received a backward pairing; and the backward groups, in turn, suppressed more than the control groups. It appears, then, that excitatory fear conditioning, as reflected in conditioned suppression of licking in rats, can be produced in a single trial by both backward and simultaneous conditioning procedures.     

One-trial context fear conditioning as a function of the interstimulus interval

In two experiments, we examined the effects of a wide range of interstimulus intervals (2.5, 15, 45, 120, 135, and 405 sec) on one-trial context fear conditioning with rats. Here, the interstimulus interval (ISI) denotes the time between placement in a conditioning chamber and the onset of a single footshock. On the conditioning day, we observed that the rats’ behavior at the time of shock onset varied systematically across ISI values. On the subsequent test day, we used context-evoked freezing as a measure of context conditioning and found the well-known inverted U-shaped ISI function. We also found that conditioned freezing for the shortest ISI values was concentrated early in the test session, whereas freezing at longer ISIs was distributed more evenly throughout the test session. The freezing results found here are more consistent with the literature on conditioning with punctate cues than are previously described results from one-trial context fear-conditioning procedures.     

Presentation of a flashing light following one-trial fear conditioning enhances retention

Rats exposed for 60 sec to a flashing light stimulus following one-trial fear conditioning showed enhanced retention performance relative to controls not exposed to the flashing light. The results of a second experiment demonstrated a time-dependent gradient of the enhancement effect. In view of additional data indicating that the flashing light is not aversive, these results suggest that the presentation of an exteroceptive stimulus can influence memory processing.     

Modulation of an activity response with associative and nonassociative fear in the rat: A lighting differential influences the form of defensive behavior evoked after fear conditioning

Rats confronted with the onset of a light gradient display a transient increase in locomotion called theactivity response (AR) and a dark preference (Godsil & Fanselow, 2004). These experiments demonstrate that the magnitude of the AR can be blunted with Pavlovian fear-conditioning procedures via associative and nonassociative fear. Although manifested in decreased locomotion, the blunted AR effect was not due to increased freezing or immobility behaviors. Instead, rats displayed reduced rearing and an increase in a class of behaviors calledstationary activity. These results suggest that the lighting differential supplied by the cue influences the topography of defensive behavior and reduces the expression of freezing. This procedure provides a means by which to examine learned and unlearned defensive responses to the same stimulus.     

Pavlovian conditioning of fear based upon hormonal mediation of prior aversive experience

A series of three experiments was conducted to determine if epinephrine administered to animals given prior shock might support learning to new environmental cues paired with the epinephrine injection. Experiment 1, utilizing nonnaive rats, provided results snowing that such learning is possible. The effect, while dose-dependent, did not appear to be based on either epinephrine-induced place aversion or on sensitization. The results of Experiment 2 confirmed the basic finding when naive animals were utilized. Experiment 3 examined more carefully the potential contribution of generalized fear, impairment of extinction of fear, and nonspecific sensitization to the phenomenon. Since the findings did not support these alternative interpretations, it appears that epinephrine administration to previously stressed rats does indeed support new learning. The epinephrine-cue association may be mediated by either of two mechanisms: (1) higher order conditioning or (2) memory reactivation. The redintegrative function of epinephrine injections, in terms of modulating memory processing, is also discussed.     

Spontaneous recovery after Pavlovian conditioning with multiple outcomes

In four experiments using rats, a Pavlovian conditioned stimulus (CS) was paired with a positive outcome, either pellets or liquid sucrose. That outcome was then either omitted altogether or replaced by another outcome. Although performance to the CS deteriorated only when the outcome was omitted, both procedures resulted in the CS’s ability to evoke greater responding after the passage of time. These results suggest that a similar outcome-independent depressive process develops when a Pavlovian CS is paired either with nonreinforcement or with a different outcome; that process then appears to dissipate with time.