Second-order conditioning of the rabbit's nictitating membrane response. Interstimulus interval and frequency of CS-CS pairings.

Second-order conditioning of the rabbit's nictitating membrane response (NMR) was investigated when second-order trials (CS1-CS2) were intermixed with first-order trials (CS2-US) from the outset of training. Experiment 1 showed that CR acquisition to CS1 was inversely related to the CS1-CS2 interval but nevertheless extended to an interval of 8,400 ms. Experiment 2 revealed that CR acquisition of CS1 was an inverted-U function of the number of CS1-CS2 trials relative to a fixed number of CS2-US trials. Experiment 3 directly contrasted second-order conditioning with a reinforced serial compound procedure (CS1-CS2-US) and a mixed procedure in which second-order trials were intermixed with the reinforced serial compound. Second-order conditioning was about half the strength of either the reinforced serial compound or the mixed procedure, which were similar. The present results are discussed with respect to the relative strength of excitatory and inhibitory processes in second-order conditioning.     

Second-order conditioning of the rabbit’s nictitating membrane response

Second-order conditioning of the rabbit’s nictitating membrane response (NMR) was investigated when second-order trials (CS1-CS2) were intermixed with first-order trials (CS2-US) from the outset of training. Experiment 1 showed that CR acquisition to CS1 was inversely related to the CS1-CS2 interval but nevertheless extended to an interval of 8,400 ms. Experiment 2 revealed that CR acquisition of CS1 was an inverted-U function of the number of CS1-CS2 trials relative to a fixed number of CS2-US trials. Experiment 3 directly contrasted second-order conditioning with a reinforced serial compound procedure (CS1-CS2-US) and a mixed procedure in which second-order trials were intermixed with the reinforced serial compound. Second-order conditioning was about half the strength of either the reinforced serial compound or the mixed procedure, which were similar. The present results are discussed with respect to the relative strength of excitatory and inhibitory processes in second-order conditioning.     

Blocking with serial compound stimuli: The role of local context and second-order associations

Blocking was studied with rats in two serial conditioning experiments in which CS1 was followed by CS2 and then shock. Experiment 1 demonstrated that pretraining with CS1 was able to block conditioning to CS2 when the pretraining consisted of trace conditioning. But when serial conditioning was used for pretraining, with a third stimulus as the second element of the compound, then blocking was not detected during the subsequent phase. In Experiment 2 the effect of pretraining with CS2 on blocking with CS1 was examined. Blocking was effective, but only when steps were taken to minimize the growth of second-order associations resulting from the pairing of CS1 with CS2. These results are consistent with a principle stating that the ability of a pretrained stimulus to block the added stimulus in a compound depends on the relative contiguity of each stimulus to the US.     

Associative transfer and stimulus selection in classical conditioning of the rabbit's nictitating membrane response to serial compound CSs

Four experiments were conducted to determine whether in conditioning to a serial compound, CS1-CS2-UCS, there are (a) associative mechanisms operating to extend conditioning beyond the bounds of a CS-UCS contiguity gradient and (b) stimulus selection processes acting to attenuate the potency of CS-UCS contiguity. In Experiments 1 and 2, the CS2-UCS interval was held at .35 sec while the CS1-UCS interval was varied across groups from .75 to 2.75 sec. CS1 test trials revealed substantial CR acquisition at all CS1-UCS intervals. Moreover, Experiment 2 indicated that when the contribution of cross-modal generalization from CS2 to CS1 was factored out, there still remained a substantial level of conditioning, which Experiment 3 indicated was attributable to an associative mechanism like higher-order or sensory conditioning. The observation of CR acquisition at CS1-UCS intervals of 4.75, 8.75, and 18.75 sec in Experiment 4 suggested that serial compound training yields conditioning to CSs located well beyond the single CS contiguity gradient for the rabbit's nictitating membrane response. Experiments 1 and 2 also indicated the presence of stimulus selection processes because, at the shorter CS1-UCS intervals (.75 and 1.25 sec), the levels of test-trial responding to CS2 fell below those observed to the less contiguous CS1.     

Cholinergic modulation of trace conditioning trained in serial compound: A developmental analysis

In four experiments the effects of serial compound conditioning on responding to a trace-conditioned CS were evaluated using a fear conditioning paradigm. The subjects were 18- and 25-day-old Sprague-Dawley rats, previously shown to exhibit little or no trace fear conditioning. Here, animals as young as 18 days of age were shown to be capable of trace conditioning between a visual CS1 and a shock US, provided the trace interval was filled with a non-target CS2 during serial conditioning trials (CS1-->CS2-->US). To explore cholinergic mechanisms involved in trace and serial conditioning, additional experiments assessed conditioned responding following pre-training administration of the muscarinic receptor antagonist scopolamine. Scopolamine produced a dose-dependent reduction in responding to the trace CS1, regardless of whether subjects were trained with standard trace (CS1-->trace interval-->US) or serial (CS1-->CS2-->US) trials. Responding to CS2 was unaffected by scopolamine. These data suggest that central cholinergic systems are functional in the young animals, but are not normally sufficiently activated by standard trace conditioning procedures. The results suggest that serial compound conditioning can promote trace conditioning in young rats, as it does in adults, perhaps by enhancing cholinergic activity during training. Implications for the late ontogenetic emergence of trace conditioning as it relates to maturation of neural pathways and their role in the potentiating effects of a gap filler are discussed.     

Element pretraining influences the content of appetitive serial compound conditioning in rats

Four experiments with rat subjects in a Pavlovian appetitive conditioning procedure examined the effects of prior pairings of S2 with the unconditioned stimulus (US) on the nature of the associations formed in S1----S2----US serial compound conditioning. Experiments 1 and 2 showed that prior training of S2 prevented the acquisition of stimulus-stimulus (S-S) associations between S1 and stimulus features of S2, but enhanced the acquisition of stimulus-response (S-R) associations between S1 and the emotional conditioned response (CR) evoked by S2. Experiments 3 and 4 showed that the effects of S2 pretraining were not due to S2 training itself, but rather to its endowing S2 with the ability to evoke a strong CR during the early stages of serial compound conditioning. In Experiment 3, suppression of the CR to a pretrained S2 during serial compound conditioning permitted the establishment of S-S associations. In Experiment 4, the induction of a CR in the presence of an untrained S2 during serial compound conditioning prevented the acquisition of S-S associations. Implications of these data for our understanding of compound conditioning are discussed.     

An analysis of second-order autoshaping

Three mechanisms can explain second-order conditioning: (1) The second-order conditioned stimulus (CS2) could activate a representation of the first-order conditioned stimulus (CS1), thereby provoking the conditioned response (CR); The CS2 could enter into an excitatory association with either (2) the representation governing the CR, or (3) with a representation of the reinforcer evoked by the CS1. A series of experiments using second-order autoshaping with birds was performed to examine these possibilities. Following second-order autoshaping, birds’ responding to the CS2 was found to be unaffected by extinction of the CS1, a result interpreted as showing mechanism (1) to be unimportant and implicating either one or both of the other mechanisms. The CS2 was also shown to provide the birds with specific sensory information about the reinforcer, a pattern of results uniquely predicted by mechanism (3). Implications for the understanding of second-order conditioning and for the SOP model (Wagner, 1981) of associative learning are discussed.     

The role of CS-US contiguity in classical conditioning of the rabbit's nictitating membrane response to serial stimuli

The rabbit's nictitating membrane response was classically conditioned to a serial tone-light compound (CS1-CS2), in which the CS1-CS2 and CS2-US intervals were each manipulated over the values of 200, 400, 800, and 1600 msec in a between-groups, factorial design. In addition, at each level of the CS2-US interval, there was a control group that received CS2 and the US. Within the serial compound, the CS2 was found to be highly efficacious in that the CS2-US interval determined the rate of CR acquisition to the compound as a whole and to CS2 in particular. Moreover, CR probability during CS2 largely overlapped the performance of the corresponding single-stimulus controls. Outside the context of the compound, CR frequency on CS2 test trials fell below control levels at the 200- and 400-msec CS2-US intervals. The results can be interpreted as indicating that a generalization decrement or information loss occurred in transferring from compound training to CS2 testing. In addition, the theories of Rescorla and Wagner (In A. Black & W. F. Prokasy, Eds., Classical conditioning II, New York: Appleton-Century-Crofts, 1972) and Mackintosh (Psychological Review, 1975, 82, 276–298) may be extended to account for the present results.     

Compound conditioning: Elimination of the blocking effect

Prior conditioning employing one element of a compound stimulus as the CS blocked the acquisition of a Conditioned Emotional Response (CER) to the second element of a simultaneous compound stimulus that was subsequently used as the CS in further conditioning trials. Presentation of a brief “surprise” stimulus 3 or 5 sec after the occurrence of the US during the compound trials eliminated the blocking effect.     

Hippocampal and cerebellar single-unit activity during delay and trace eyeblink conditioning in the rat

In delay eyeblink conditioning, the CS overlaps with the US and only a brainstem-cerebellar circuit is necessary for learning. In trace eyeblink conditioning, the CS ends before the US is delivered and several forebrain structures, including the hippocampus, are required for learning, in addition to a brainstem-cerebellar circuit. The interstimulus interval (ISI) between CS onset and US onset is perhaps the most important factor in classical conditioning, but studies comparing delay and trace conditioning have typically not matched these procedures in this crucial factor, so it is often difficult to determine whether results are due to differences between delay and trace or to differences in ISI. In the current study, we employed a 580-ms CS-US interval for both delay and trace conditioning and compared hippocampal CA1 activity and cerebellar interpositus nucleus activity in order to determine whether a unique signature of trace conditioning exists in patterns of single-unit activity in either structure. Long-Evans rats were chronically implanted in either CA1 or interpositus with microwire electrodes and underwent either delay eyeblink conditioning, or trace eyeblink conditioning with a 300-ms trace period between CS offset and US onset. On trials with a CR in delay conditioning, CA1 pyramidal cells showed increases in activation (relative to a pre-CS baseline) during the CS-US period in sessions 1-4 that was attenuated by sessions 5-6. In contrast, on trials with a CR in trace conditioning, CA1 pyramidal cells did not show increases in activation during the CS-US period until sessions 5-6. In sessions 5-6, increases in activation were present only to the CS and not during the trace period. For rats with interpositus electrodes, activation of interpositus neurons on CR trials was present in all sessions in both delay and trace conditioning. However, activation was greater in trace compared to delay conditioning in the first half of the CS-US interval (during the trace CS) during early sessions of conditioning and, in later sessions of conditioning, activation was greater in the second half of the CS-US interval (during the trace interval). These results suggest that the pattern of hippocampal activation that differentiates trace from delay eyeblink conditioning is a slow buildup of activation to the CS, possibly representing encoding of CS duration or discrimination of the CS from the background context. Interpositus nucleus neurons show strong modeling of the eyeblink CR regardless of paradigm but show a changing pattern across conditioning that may be due to the necessary contributions of forebrain processing to trace conditioning.     

Blocking acquisition of the rabbit's nictitating membrane response to serial conditioned stimuli

Three experiments demonstrated that prior training with one stimulus (CS1) would block acquisition of the rabbit's nictitating membrane response (NMR) to another stimulus (CS2) which was more contiguous to the US during serial compound training (CS1-CS2-US). Specifically, the CS1-US interval was 800 msec, which produces only a modest rate of CR acquisition, while the CS2-US interval was 400 msec, which is an optimal value for the NMR preparation. Experiment 1 demonstrated blocking when CS1 overlapped CS2, and Experiment 3 demonstrated blocking when CS1 and CS2 were presented in a strictly sequential fashion. Experiment 2 showed that the magnitude of blocking in the serial compound was comparable to that obtained in a simultaneous compound in which both the CS1-US and CS2-US intervals were 800 msec, thus making CS2 less contiguous with the US than in the serial compound. Moreover, the level of responding to CS2 in all serial compound groups (blocking and control) was lower than in the simultaneous compound groups. The present findings provide further evidence that the associative consequences of CS-US contiguity can be highly attenuated by processes of attention or competition for associative strength.     

The influence of partial reinforcement on serial autoshaping with pigeons

The effect of partial reinforcement on the rate of responding during the first element of a serial compound was investigated using autoshaping in pigeons. Experiment I employed the illumination of a response key by two different colours as the elements of the compound. Responding during the first element was faster when this stimulus was intermittently paired with the second element and the unconditioned stimulus than when a continuous reinforcement schedule was employed. Experiment II demonstrated that this effect of partial reinforcement is unaffected by maniuplating the associative strength of the second element at the outset of compound conditioning. A similar effect of partial reinforcement was also found in Experiment III which used a tone as the first element of the serial compound.     

Pavlovian second-order conditioned analgesia

Three experiments with rat subjects assessed conditioned analgesia in a Pavlovian second-order conditioning procedure by using inhibition of responding to thermal stimulation as an index of pain sensitivity. In Experiment 1, rats receiving second-order conditioning showed longer response latencies during a test of pain sensitivity in the presence of the second-order conditioned stimulus (CS) than rats receiving appropriate control procedures. Experiment 2 found that extinction of the first-order CS had no effect on established second-order conditioned analgesia. Experiment 3 evaluated the effects of post second-order conditioning pairings of morphine and the shock unconditioned stimulus (US). Rats receiving paired morphine-shock presentations showed significantly shorter response latencies during a hot-plate test of pain sensitivity in the presence of the second-order CS than did groups of rats receiving various control procedures; second-order analgesia was attenuated. These data extend the associative account of conditioned analgesia to second-order conditioning situations and are discussed in terms of the mediation of both first- and second-order analgesia by an association between the CS and a representation or expectancy of the US, which may directly activate endogenous pain inhibition systems.     

The effect of on‐ or off‐line extinction of a first‐order conditioned stimulus on a second‐order conditioned response in rats

In a water‐licking experiment with rats, the effects of the extinction of a first‐order conditioned stimulus (CS1) on the suppression of licking established for a second‐order conditioned stimulus (CS2) were explored. Extinction of the first‐order conditioned response (CR1) attenuated the conditioned suppression induced by CS2 when the rats had been allowed to lick water during the CR1 extinction phase. However, if water had been unavailable during the CR1 extinction phase, suppression by CS2 was not affected. The latter result is consistent with other studies of rats' conditioned suppression and suggests that the underlying mechanism of second‐order conditioning in this experiment is a connection between CS2 and the response elicited by CS1 rather than a CS2‐CS1 connection. The former result was interpreted as the CR1 extinction phase encouraging the rats to lick water despite the fear elicited by CS1, and thus, in testing, they licked despite the fear elicited by CS2.     

Conditioning of the rabbit's nictitating membrane response to a CSA-CSB-US serial compound: manipulations of CSB's associative character.

Response acquisition to a trace conditioned stimulus (CSA) can be facilitated by insertion of a second stimulus (CSB) at the end of the trace interval just before the unconditioned stimulus (US). This effect may arise from serial mediation of trace conditioning, second-order conditioning, or both. Whereas serial mediation relies only on the presence of CSB, associative transfer relies on CSB's associative strength. In the present experiments, the presence of CSB was fixed, whereas CSB's associative strength was manipulated by (a) extinction of CSB, (b) latent inhibition of CSB, and (c) prior CSB-US pairings. In the first 2 cases, the level of responding to CSA was reduced in a fashion parallel to that of CSB. However, in the third case, partial blocking of conditioned response (CR) acquisition to CSA was observed. The results are discussed with reference to the role of associative transfer to both facilitating and blocking CR acquisition to CSA.     

Role of the hippocampus in blocking and conditioned inhibition of the rabbit's nictitating membrane response.

Bilateral aspiration of the dorsal hippocampus produced a disrupttion of blocking of the rabbit's nictitating membrane response in Kamin's two-stage paradigm (Experiment 1) but had no effect on the formation of a Pavlovian conditioned inhibitor (Experiment 2). The results of Experiment 1 indicated that normal animals and those with cortical lesions given conditioning to a light-plus-tone conditioned stimulus (CS) gave conditioned responses (CRs) to both the light and the tone during nonreinforced presentations of each (test phase). If, however, compound conditioning was preceded by tone acquisition, only the tone elicited a CR during testing; that is, blocking was observed. In rabbits with hippocampal lesions, however, CRs were given to both the light and the tone during testing whether or not compound conditioning was preceded by tone acquisition. The data from Experiment 2 showed that rabbits with hippocampal lesions could discriminate as well as normal rabbits and those with cortical lesions between a light (CS+) and light plus tone (CS-). In addition, when the inhibitory tone was subsequently paired with the unconditioned stimulus in retardation testing, animals in all three lesion conditions acquired the CR at the same rate. Thus, it appears that hippocampal lesions do not disrupt conditioned inhibition. The results of these experiments were taken as support for the view that the hippocampus is responsible for "tuning out" stimuli that have no adaptive value to the organism.     

The problem of switching in conditional behavior

This article reviews studies of various authors on the phenomenon of “switching,” which is observed in both classical and instrumental conditioning and consists in elicitation of different responses to the same conditional stimulus (CS) when it is applied in an environment different than the original one. The different responses include a decrease or an absence of the previously trained conditional response (CR), elicitation of an appetitive response instead a defensive one, or vice versa, as well as elicitation of two different instrumental CRs in the same trial. The studies suggest that, due to the repeated occurrence of CS in the same environment (E), also called “situation” or “context,” associations are formed between CS and E. Consequently, the CR is elicited to a compound CS+E rather than to CS alone. When the CS is applied alone in a different E than the original one, the previously formed associations are inactive and the CR cannot be elicited; this leads to switching. Studies also suggest that E plays a dominant role in conditioning compared with that of CS alone, which often appears to be only a trigger for eliciting the response. However, CS tested in a different E may still produce some components of the previously acquired CR, such as a general fear behavior to an originally defensive CS or an approach behavior to an originally alimentary CS. The environmental stimuli can be considered the “determining” stimuli that determine the kind of reaction to be elicited, or “tonic” stimuli that increase the tonus in the brain but do not elicit the CR. The “determining” or “tonic” stimuli do not seem to be a special class of stimuli. Instead, they are stimuli that initially can produce the CR (e.g., intertrial CRs), but by being not reinforced they become partly inhibited; nevertheless, due to associations with the reinforcement, they still can produce some excitement related to it, thus facilitating the CR.     

Pavlovian conditioning of sexual arousal: first- and second-order effects

Despite the likely importance of Pavlovian conditioning in sexual behavior, previous evidence of reliable or sizeable effects is very sparse. This report includes four experiments in the conditioning of sexual arousal in the males of a mammalian species, namely, the rat. In each case the unconditioned response (UR) was unconsummated arousal after exposure to a female. There was evidence of a substantial conditioned effect, as shown by decreases in the time to complete copulation during postconditioning conditioned stimulus (CS) tests. It is also possible to establish a second-order conditioned response (CR), which retains its strength even after extinction of the first-order response. These results confirm the power of Pavlovian contingencies in sexual responding and provide implications for conditioning theory and applied work.     

Contextual conditioning in infants, but not older animals, is facilitated by CS conditioning

Context conditioning in infant Sprague-Dawley rats (postnatal days [PD] 15, 17, and 19), juveniles (PD 25), adolescents (PD 35), and adults (PD 71-89) was compared when CS conditioning did or did not occur in the context. Degree of CS conditioning within that context was equated across age, and separate groups at each age were given unpaired presentations of the CS and US within that context. Infants conditioned more effectively to context when CS-US pairings occurred in that context than when they did not, juveniles conditioned to context about equally with and without CS-US pairings in the context, and adolescents and adults conditioned less effectively to context when CS and US were paired than when unpaired. Adolescents had significant context conditioning despite CS-US pairings in the context but adults did not, and overall, context conditioning was strongest for adolescents. Supplementary experiments indicated that with more extensive conditioning experience, the infants' pattern of context conditioning became more similar to that of older animals, and with less conditioning experience the pattern of context conditioning by adults became more similar to that of younger animals, but infants never attained the adult pattern of context conditioning nor did adults attain the infant pattern. The potentiation of context conditioning by CS conditioning observed in infants is consistent with previous evidence derived from compound conditioning. Alternative explanations place common emphasis on infant-specific amodal processing. One views potentiation as a result of the greater perceived intensity of the stimulus compound (CS and context, in this case) during conditioning and the lesser generalization decrement in infants than adults when tested with a single element after conditioning with a compound. The other explanation emphasizes consequences of the redundancy inherent in intersensory compounds, within the theory of Bahrick and Lickliter.     

The effects of cued UCS rehearsal on the retention of differential 'fear' conditioning: an experimental analogue of the 'worry' process

This study describes a human electrodermal conditioning experiment in which subjects were asked to mentally rehearse the UCS in a period following initial fear conditioning and prior to a test period involving nonreinforced presentations of the CS. Subjects who were asked to rehearse the UCS retained a differential fear CR during subsequent unreinforced presentations of the CS, but control subjects who were asked to rehearse either a nonaversive event or an aversive event unrelated to the UCS failed to retain the differential CR they had acquired during conditioning. These results suggest that rehearsal of the UCS during periods when CS and UCS are absent can aid the persistence of a fear CR in the absence of further pairings of the CS and UCS. It is argued that these effects can be explained in terms of the effect of UCS rehearsal on the strength and evaluation of the UCS representation. It is also suggested that cued UCS rehearsal might provide a useful procedure for understanding clinical incubation effects and for understanding how the 'worry' process contributes to the maintenance and incubation of fear.