Integration of cardiac responses to serial stimuli after Pavlovian conditioning in rats

The expression of cardiac responses to sequences of two sounds was studied in restrained rats following discriminative trace or delay conditioning. Stimuli paired with a tail shock 10 sec later (CS1) elicited conditioned bradycardia. Unpaired or neutral stimuli (CS0) elicited mostly tachycardia. Rats did not learn to suppress responding to nonreinforced sequences with an interval of 6 sec between sounds. Responses to the second stimulus were significantly augmented following a CS1 stimulus, but not following a CS0 stimulus. Real-time summation of simple responses provided a more complete and quantitative prediction of dual responses than did resetting or facilitation. These results extend the time range over which summation may be observed from less than 2 sec to at least 16 sec. They appear to be inconsistent with models involving competition between unitary representations of stimuli in short-term memory and suggest the existence of multiple stimulus traces with independent time courses.     

Facilitation of licking by response-contingent electric shock

Licking behavior of rats maintained by lick-contingent water reinforcement, produced electric shocks under three conditions. Shock occurred 1 sec before, simultaneous with, or 1 sec after water reinforcement. Rates of licking rose above prepunished levels at .2-, .4-, and .6-mA intensities but were suppressed at .8 mA for all three groups. Facilitation and suppression effects were the same for the three pairing conditions. Discriminative and elicited functions of shock did not appear to account for this facilitative effect.     

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

Rats received a single 4-sec 1-mA grid-shock US either preceded or followed by a 4-sec tone or light CS. Conditioning was later assessed by comparing the amount of lick suppression evoked by the forward- or backward-paired CS versus an explicitly unpaired CS. The backward-paired CS produced more suppression than the unpaired CS only when both were tone; the light evoked strong suppression whether paired or not. In the forward procedure, tone produced more suppression when paired and less when unpaired than did light; conditioning thus appeared stronger with the tone. In one experiment, observations showed that rats froze during the forward-paired tone but not during the light. Increasing CS duration from 4 to 12 sec had no effect for the forward-paired light but increased freezing to the forward-paired tone. Another experiment showed similar unconditioned suppression to tone and light but faster habituation to tone. Problems that these results create for interpreting evidence for excitatory backward conditioning in the conditioned suppression procedure are discussed.     

The effects of qualitative and quantitative variation in the US on individual components of Pavlovian appetitive conditioned behavior in rats

The form of rats’ Pavlovian conditioned responses to visual and auditory conditioned stimuli (CSs) paired with a variety of unconditioned stimuli (USs) was examined in three experiments using direct behavioral observation techniques. In Experiment 1, the form of conditioned behavior occurring most frequently during later portions of the CS-US interval depended only on which of several appetitive USs was used, but the form of behavior occurring most frequently during early portions of the CS-US interval depended only on the nature of the CS. US-dependent behaviors resembled the response to the US, and CS-dependent behaviors resembled the original orienting response (OR) to the CS. In Experiment 2, the use of larger magnitude appetitive USs resulted in higher frequencies of US-dependent behaviors, but lower frequencies of CS-dependent behaviors in the presence of auditory and visual CSs. In Experiment 3, US-dependent conditioned behavior to auditory and visual CSs paired with shock was more frequent when high-intensity shocks were used, but CS-dependent behavior was more frequent when low-intensity shocks were used. These results suggested that Pavlovian conditioned responding may involve two independent types of behavior—one appropriate to the US and another based on the original OR to the CS.     

Two components of responding in Pavlovian lick suppression

The present research examined the temporal distribution of responding in a lick suppression paradigm. In Experiment 1, rats were trained with either a 30- or a 120-s conditioned stimulus (CS), which was followed either by a footshock (unconditioned stimulus [US]) or nothing. Licking during the CS was suppressed only in the former condition. Suppression was more pronounced early in the CS. In Experiment 2, rats were exposed to two 30-s or two 120-s CSs, with delivery of the shock being contingent on CS1 for half of the animals and on CS2 for the other half. For both the paired and the unpaired conditions, suppression at the beginning of CS1 was observed for all the groups. By discounting the possibility of generalization between CS1 and CS2, it appears that this initial suppression was not a conditioned response to the CS, but an unconditioned one due to mere exposure to the shock US.     

Footshock-produced excitation and inhibition of activity in rats

Hooded rats received five 1-sec shock presentations of 0.3, 0.5, or 1.0 mA. Activity measures recorded during each 30-sec intershock interval and at various retention intervals (.10, 2.5, and 24 h) following footshock (FS) indicated that (a) 5 sec after FS activity is directly related to shock intensity, while 10–30 sec following FS activity is inversely related to shock intensity; (b) the rate of decline in activity following FS increases with successive shock presentations; (c) activity is greater 10 h after FS than at a 2.5- or 24-h retention interval; and finally (d) shock compartment confinement increased activity and resulted in a substantial alteration in the form of retention curve in the 0.3-mA group but had lesser effects upon the retention curves of the 0.5- and 1.0-mA groups. The data were interpreted as supporting the hypothesis that the “incubation effect” is a result of a decline of the activating effects of FS.     

Posttrial effects of presenting vs. omitting expected shock USs in the conditioned suppression procedure: Concurrent measurement of barpress suppression and freezing

Barpress suppression in a 1-min interval following CS trials was investigated using 16 rats in a conditioned suppression procedure with a two-stage design. For one group, each CS co-terminated with a brief shock US in Stage 1; then, in Stage 2, only half the CSs ended with a shock, which in turn was followed 1 min later by a second shock. For a second group, the two stages were reversed. When CSs were followed by single shocks in Stage 1, posttrial suppression weakened across trials; but when, in Stage 2, double shocks followed half the CSs, posttrial suppression grew stronger. When half the trials were followed by double shocks in Stage 1, posttrial suppression was maintained at initial levels but weakened in Stage 2 when single shocks followed each trial. In both stages, posttrial suppression was stronger on nonreinforced than on reinforced trials. Two factors were hypothesized to control posttrial suppression. First, posttrial suppression weakens with training under the single-shock procedure because post-shock temporal stimuli come to inhibit fear unless themselves paired with shock. Second, posttrial suppression is stronger on nonreinforced trials than on reinforced trials because freezing behaviors initiated during the CS are not disrupted by a US and so persist into the posttrial interval.     

Retention of conditioned autonomic and behavioral responses in preweanling rats: Forgetting and reinstatement

Preweanling rats, 16 days of age, responded to an olfactory conditioned stimulus (CS) paired with a shock unconditioned stimulus (US) with increases in heart rate and behavioral activation. In two experiments this finding was replicated and, in addition, it was found that the form of these conditioned responses (CRs) changed after a retention interval. When tested 24 h after CS-US pairings, the subjects displayed a decrease in heart rate accompanied by CS-elicited freezing. Giving two unsignaled shocks prior to the delayed test effectively reinstated the tachycardia and behavioral arousal CRs. The results are discussed in terms of contextual influences on the form of the CR and how changes in the magnitude of context fear may alter responding to an olfactory CS.     

Trial spacing effects in pavlovian conditioning: A role for local context

Two conditioned lick-suppression experiments with rats were conducted in order to replicate and extend findings by Ewing, Larew, and Wagner (1985). Ewing et al. observed that excitatory responding to a CS paired with a footshock US was attenuated when the ITIs thatpreceded each CS-US trial were short (60 sec) relative to when they were long (600 sec). This effect was isolated in the influence of the preceding ITI because the preceding ITI was consistently short for one CS and consistently long for a different CS, while the following ITIs were equally often short and long for both CSs. Ewing et al. interpreted this finding in the framework of Wagner’s (1981) SOP model. Experiment 1 replicated this trial-spacing effect and demonstrated a similar effect under conditions in which thefollowing ITI was consistently short for one CS and consistently long for a different CS, while the durations of preceding ITIs were equally often short and long for both CSs. Experiment 2 revealed that the detrimental effect of a short preceding or a short following ITI could be alleviated by extinguishing the conditioning context after CS-US training. The latter observation indicates that the trial-spacing effect is not mediated by a failure of a CS trained with a short ITI to enter into excitatory associations with the US, a conclusion that is not wholly consistent with the SOP model. Finally, we suggest that short pretrial and short posttrial ITIs may enhance the excitatory value of local context cues that modulate responding to a CS.     

Differential response gradients to a Pavlovian safety signal following active avoidance training in young and adult rats

Following 300 training trials in two-way shuttle avoidance signaled by a tone (CS+), two groups each of weanling and adult rats were given Pavlovian discrimination training in which the CS+ was followed by inescapable shock, and a more intense tone (CS—) signaled no shock. An additional group at each age level received both tones paired randomly with shock or no shock. Subsequent generalization tests along the frequency dimension indicated that both pups and adults tested at the CS+ intensity showed similar gradients of frequency control. Gradients for the adults tested at the CS — intensity tended to be inverted, with least responding at CS—, a result not found in the young subjects. The results were considered in light of Pavlovian extradimensional influences on the control of avoidance behavior.     

The effects of separate presentations of the US on conditioned suppression

Four experiments examined the effects of separate presentations of shock on conditioned suppression of instrumental responding evoked by a CS previously paired with shock. Experiment 1 showed that conditioned suppression of responding resulting from noise-shock pairings increased as a function of time after the initial noise-shock pairings. However, it also showed that this time-dependent increase in conditioned suppression of responding could be attenuated by presentations of light-shock pairings immediately prior to the test of the noise CS. Experiment 2 showed that this attenuation effect can be produced by presentations of either light-shock pairings or shock alone. Experiment 3 showed that the magnitude of this attenuation effect was directly related to the temporal proximity of the light-shock pairings to the test of the noise CS. Experiment 4 showed that the magnitude of this attenuation effect was inversely related to the intensity of separate shock presentations.     

One-trial excitatory backward conditioning as assessed by conditioned suppression of licking in rats: Concurrent observations of lick suppression and defensive behaviors

Twenty-eight male albino rats were given a single 4-sec 1-mA electric-grid-shock unconditioned stimulus (US). In the same session they received two 12-sec conditioned stimuli (CSs). One CS (explicitly unpaired) terminated 180 sec before the US began; the other (backward paired) began immediately after the US terminated. The CSs used were a 1000-Hz 85-dB tone and an 84-dB click; their roles were counterbalanced. Over the next 2 days, each CS was presented for 2 min while the rats drank from a water bottle. The backward-paired CS was found to suppress licking more than the explicitly unpaired CS. This suppression was accompanied by an increase in defensive behavior (freezing and freeze/nod) and by a decrease in other activity. The suppression did not seem to be due to a maintained or enhanced CS-orienting response reflex, nor could it be attributed to an adventitiously reinforced interfering operant. The results support the presumption made in previous reports that the lick suppression evoked by a backward CS reflected one-trial backward excitatory fear conditioning.     

Fear of the CS and of the context in two-way avoidance learning: Between- and within-subjects manipulations

The roles of CS fear and of context fear in signaled two-way avoidance learning were examined in two experiments in which shock intensity was manipulated either between or within subjects. For each subject, two discrete CSs, a light and a white noise, were used. For between-subjects comparisons, both CSs were paired with the same shock intensity, weak or strong. Under this condition, in which fear of the CSs and the context was greater with strong than with weak shock, avoidance performance varied inversely with shock intensity. For within-subjects comparisons, the light was paired with strong shock and the white noise with weak shock, or vice versa. In this case, context fear was constant during presentation of each CS, and avoidance performance varied directly with shock intensity. Additionally, intertrial responding was directly related to the amount of context fear. These results support effective reinforcement theory, an extension of two-factor theory, which acknowledges the contribution to avoidance learning both of CS fear and of context fear. The interchangeable effectiveness of visual and auditory stimuli as CSs is discussed with regard to stimulus specificity in avoidance learning.     

Short-term retention of “surprising” events following different training conditions

Terry and Wagner (1975) have suggested that short-term retention of information about an event is enhanced if the occurrence of the event is surprising. To investigate this idea, we trained two groups of pigeons in a preparatory-releaser procedure in which half the trials started with the presentation of food (the preparatory event). The preparatory food presensation was signaled by an 8-sec white keylight in the signaled, but not in the unsignaled, group. After a retention interval, varying between 2 and 32 sec, the releaser stimulus (CS_R), a red keylight, was presented for 8 sec in the absence of any reinforcement. The remaining trials were initiated by the presentation of CS_R, and the first peck occurring 8 sec after the onset of CS_R was reinforced by food. The preparatory event controlled responding to CS_R at the short retention interval, with the level of control declining systematically with increasing retention intervals. On probe test trials, the presentation of the preparatory food event was preceded by a stimulus that had previously been paired (CS+) or unpaired with food (CS?). Discriminative responding to CSr was better following CS? than following CS+ in the unsignaled, but not the signaled, group. These results suggest that the enhanced retention following surprising preparatory events reflects a generalization decrement induced by changing the signaling conditions between training and testing.     

CS preexposure: Latent inhibition and Pavlovian conditioning of heart rate and eyeblink responses as a function of sex and CS intensity in rabbits

Male and female rabbits received Pavlovian conditioning in which a 1, 216-Hz tone served as the CS and a 3-mA paraorbital electric shock train served as the US. Eyeblink (EB) and heart rate (HR) CRs were assessed. Half of the animals received prior exposure to the CS, while half were restrained in the chamber for a similar length of time but did not receive prior CS exposure. Different groups of each sex received three different CS intensities including 60, 75, and 90 dB (SPL) during both preexposure and conditioning. The results revealed that latent inhibition of the EB CR occurred only at the intermediate CS intensity, as indicated by a significant impairment of EB conditioning in this group. However, the magnitude of the decelerative HR CR was attenuated by prior CS exposure at all three CS intensities. Females showed faster EB conditioning than males, but latent inhibition occurred in both sexes. These results suggest that somatomotor and autonomic systems are affected differently by prior CS exposure.     

Classical conditioning in paramecia

SingleParamecium caudatum were conditioned by pairing ac-generated electric shock (US) with a vibratory stimulus (CS) produced by an auditory speaker. Naive paramecia subjected to shock reliably exhibited a backwards jerk and axial spinning similar to the avoiding reaction described by Jennings in 1904. Such responses did not occur initially to CS alone, but increasingly appeared during the CS period preceding shock pairing (delayed conditioning paradigm). Control subjects given the CS and UCS at the same intervals, but explicitly unpaired, did not show a sustained increase of responses to the CS alone. Short-term memory was demonstrated by subjects first conditioned and then presented CS alone during extinction. These subjects were readily reconditioned. Paramecia trained and stored for 24 h showed reliable memory savings as compared to stored control subjects. Other paramecia were differentially conditioned by training with two CSs. Following the recommendations of Rescorla (1967), a procedure was designed for truly random presentation of the CS and UCS as an additional control for pseudoconditioning. Single paramecia were conditioned with intervals between CSs randomly ranging from 8 to 32 sec. Control subjects received the same number of CSs and UCSs, which were administered independently and randomly during the same total session duration. Thus, CS and UCS were occasionally paired for control subjects. The responses to CS in the conditioned group were anticipatory conditional responses due to the pairing contingency and not wholly due to pseudoconditioning.     

Trial and intertrial durations in appetitive conditioning in rats

The effects of trial (T) and intertrial (I) durations were examined in two Pavlovian conditioning experiments with rats, in which a noise conditioned stimulus (CS) was paired with food delivery. In Experiment 1,T was either 10 or 20 sec, andI ranged from 15 to 960 sec, in separate groups of rats. The acquisition rate and final level of conditioned responding showed ratio invariance: They were better predicted by theI/T ratio than byI orT alone. In Experiment 2, theI/T ratio was 6.0 in all the groups, andT was 20, 40, 80, or 160 sec. Ratio invariance was not observed: Despite the commonI/T ratio, the rate of acquisition, final level of conditioned responding, and the ability of the CS to block conditioning of another stimulus differed among the groups. At the same time, the temporal distribution of conditioned responding withinT was similar in all the groups throughout conditioning and extinction and showed superpositioning when normalized acrossT. Many but not all aspects of the data were consistent with scalar timing theory.     

Bidirectional avoidance by mice as a function of CS,US, and apparatus variables

Acquisition of two-way avoidance by mice was slower with a light CS than with a buzzer CS, with punishment of intertrial responses than without punishment, and with a short CS-CS interval than with a long CS-CS interval (30 vs. 60 sec). Light-cued avoidance was little affected by shock level (.35–1.5 mA), whereas mice trained with the buzzer CS learned faster at 1.5 mA. Animals required to move away from light or toward light showed comparable rates of acquisition. Other CS, US, and apparatus variables (directionality of cue, maximal shock duration, and presence vs. absence of a central partition in the shuttlebox) interacted in a complex fashion with those already mentioned. This resulted in widely differing performances in what may superficially appear to be different versions of the same task. The differences in mouse and rat responses to some of the variables can contribute to an understanding of the interactions between organismic and test factors and the relative explanatory value of alternative avoidance models.     

Effects of US parameters on classical conditioning of cat hindlimb flexion

Unconditioned stimulus (US) intensity and duration were manipulated to determine their effects on cat hindlimb flexion conditioning. Seven consecutive days of acquisition training of a hindlimb flexor response to a tone conditioned stimulus (CS) were followed by 2 days of extinction. Eight animals in each of 12 groups received a 1-, 2-, 3-, or 4-mA, 60-Hz shock delivered to the right hindleg for 25, 50, or 100 msec as the US. Analysis of conditioned-response (CR) frequency indicated that conditioned responding was a positive function of both the intensity and duration of shock, although these variables did not interact with one another. CR latency and amplitude were decreased and increased, respectively, by increases in US intensity. The pattern of results reported here may support a contiguity notion of conditioning, and are discussed in the context of other conditioning preparations.     

The influence of shock during response prevention upon resistance to extinction of an avoidance response

A recent study found that avoidance extinction is equally facilitated by response prevention (blocking) whether the latter involves CS-alone or CS-shock presentations. An experiment was performed to determine whether this result was due to the use of a lengthy shock (5 sec) during response prevention. Five groups of rats were extinguished: (1) without prior blocking, (2) after blocking with CS only, (3) after blocking with a lengthy (5 sec) CS-contingent shock, (4) after blocking with a brief (.5 sec) CS-contingent shock, or (5) after blocking with a brief (.5 sec) shock only. The group blocked with the brief CS-contingent shock was substantially more resistant to extinction than the other four groups. The unblocked group and the group blocked with brief shock only required more trials to extinguish than the groups blocked with CS only or with lengthy CS-contingent shock, but did not differ from each other. The groups blocked with CS only or with lengthy CS-contingent shock also failed to differ from one another. The data support a significant role for Pavlovian conditioning processes in the effect of response prevention upon avoidance extinction.