Retention of Conditioned Inhibition Produced by Extinction

Rats in a flavor aversion procedure were used to examine the extent to which an extinguished CS can pass a retardation and summation test for conditioned inhibition after either a short or a long retention interval. Rats were given a single pairing of a flavored solution with LiCl, and then received a large number of CS-alone extinction trials. Following extinction, some subjects received a 3-week retention interval following extinction while others did not. Extinction produced evidence of conditioned inhibition on both tests when a short retention interval occurred following extinction. However, conditioned inhibition was attenuated by the long retention interval when assessed with a retardation test, but no effect of the long retention interval was observed when inhibition was evaluated with a summation test.     

Forgetting of conditioned fear inhibition

Three experiments assessed retention of conditioned fear and of fear inhibition over long-term retention intervals (35 days in two experiments, 25 days in the third). Although excitatory conditioning was retained well, conditioned inhibition was not. This effect occurred when inhibition was assessed by compounding stimuli on an appetitive baseline and when it was assessed by testing cues on a baseline of unsignalled avoidance responding. Inhibition was also forgotten when the initial conditioning treatment was designed to reduce the role of possible proactive interference processes.     

Conditioned Inhibition Produced by Extinction of a Conditioned Stimulus

Four experiments used a conditioned taste aversion procedure to examine the potential for CS-alone extinction treatment to produce a conditioned stimulus that possesses inhibitory properties. In Experiment 1, saccharin was paired with LiCl, and then saccharin was presented alone for several trials to produce extensive behavioral extinction. Animals receiving this treatment were retarded in reacquiring conditioned responding to saccharin relative to control subjects receiving conditioning to the flavor for the first time. In Experiment 2, the extinguished saccharin stimulus was shown to decrease conditioned responding to a known excitor when the two stimuli were presented in compound as a summation test. Experiments 3A and 3B replicated the findings of Experiments 1 and 2 while providing evidence that the effects were not due to the differential effects of neophobia during testing. These three experiments revealed that an extinguished conditioned excitor passes retardation and summation tests for conditioned inhibition. Experiment 4 found that extinction of a known excitor was slowed when the excitor was extinguished in compound with a previously extinguished conditioned stimulus. That is, an extinguished CS provided protection from extinction to another CS, a finding also consistent with the view that extinction produces conditioned inhibition.     

Temporal coding in conditioned inhibition: analysis of associative structure of inhibition

Two experiments with rats as subjects were conducted to investigate the associative structure of temporal control of conditioned inhibition through posttraining manipulation of the training excitor-unconditioned stimulus (US) temporal relationship. Experiment 1 found that following simultaneous Pavlovian inhibition training (i.e., A --> US/XA-no US) in which a conditioned stimulus (CS A) was established as a delay excitor, maximal inhibition was observed on a summation test when CS X was compounded with a delay transfer CS. Furthermore, posttraining shifts in the A-US temporal relationship from delay to trace resulted in maximal inhibition of a trace transfer CS. Experiment 2 found complementary results to Experiment 1 with an A-US posttraining shift from serial to simultaneous. These results suggest that temporal control of inhibition is mediated by the training excitor-US temporal relationship.     

Perirhinal cortex lesions impair feature-negative discrimination

The role of the perirhinal cortex in inhibitory eyeblink conditioning was examined. In Experiment 1, rats were given lesions of the perirhinal cortex or control surgery and subsequently trained with a feature-negative discrimination procedure followed by summation and retardation tests for conditioned inhibition. Perirhinal cortex lesions impaired, but did not prevent acquisition of feature-negative discrimination. Results from the summation test showed that rats with perirhinal cortex lesions could not generalize feature-negative discrimination to a new stimulus. There were no group differences during the retardation test. Experiment 2 showed that lesions of the perirhinal cortex did not impair simple excitatory conditioning. Experiment 3 showed that perirhinal cortex lesions had no effect on acquisition of a simple tone-light discrimination. The results suggest that the perirhinal cortex plays a role in eyeblink conditioning when using discrimination procedures involving overlapping stimuli.     

Blockade of GABAA receptors in the interpositus nucleus modulates expression of conditioned excitation but not conditioned inhibition of the eyeblink response

The cerebellum and related brainstem structures are essential for excitatory eyeblink conditioning. Recent evidence indicates that the cerebellar interpositus and lateral pontine nuclei may also play critical roles in conditioned inhibition (CI) of the eyeblink response. The current study examined the role of GABAergic inhibition of the interpositus nucleus in retention of CI. Male Long-Evans rats were implanted with a cannula positioned just above or in the anterior interpositus nucleus before training. The rats were trained with two different tones and a light as conditioned stimuli, and a periorbital shock as the unconditioned stimulus. CI training consisted of four phases: 1) excitatory conditioning (8 kHz tone paired with shock); 2) feature-negative discrimination (2 kHz tone paired with shock or 2 kHz tone concurrent with light); 3) summation test (8 kHz tone or 8 kHz tone concurrent with light); and 4) retardation test (light paired with shock) After reaching a criterion level of performance on the feature-negative discrimination (40% discrimination), 0.5 μl picrotoxin (a GABA_A receptor antagonist) was infused at one of four concentrations, each concentration infused during separte test sessions. Picrotoxin transiently impaired conditioned responses during trials with the excitatory stimulus (tone) in a dose-dependent manner, but did not significantly impact responding to the inhibitory compound stimulus (tone-light). The results suggest that expression of conditioned inhibition of the eyeblink conditioned response does not require GABAergic inhibition of neurons in the anterior interpositus nucleus.     

Blockade of GABAA Receptors in the Interpositus Nucleus Modulates Expression of Conditioned Excitation but not Conditioned Inhibition of the Eyeblink Response

The cerebellum and related brainstem structures are essential for excitatory eyeblink conditioning. Recent evidence indicates that the cerebellar interpositus and lateral pontine nuclei may also play critical roles in conditioned inhibition (CI) of the eyeblink response. The current study examined the role of GABAergic inhibition of the interpositus nucleus in retention of CI. Male Long-Evans rats were implanted with a cannula positioned just above or in the anterior interpositus nucleus before training. The rats were trained with two different tones and a light as conditioned stimuli, and a periorbital shock as the unconditioned stimulus. CI training consisted of four phases: 1) excitatory conditioning (8 kHz tone paired with shock); 2) feature-negative discrimination (2 kHz tone paired with shock or 2 kHz tone concurrent with light); 3) summation test (8 kHz tone or 8 kHz tone concurrent with light); and 4) retardation test (light paired with shock). After reaching a criterion level of performance on the feature-negative discrimination (40% discrimination), 0.5 microl picrotoxin (a GABAA receptor antagonist) was infused at one of four concentrations, each concentration infused during separate test sessions. Picrotoxin transiently impaired conditioned responses during trials with the excitatory stimulus (tone) in a dose-dependent manner, but did not significantly impact responding to the inhibitory compound stimulus (tone-light). The results suggest that expression of conditioned inhibition of the eyeblink conditioned response does not require GABAergic inhibition of neurons in the anterior interpositus nucleus.     

Odor as a conditioned inhibitor: Applicability of the Rescorla-Wagner model to feeding behavior

Hooded rats were given conditioned inhibition training in which the taste of saccharin alone was always followed by induced illness, but the taste of saccharin plus the odor of amyl acetate was not. In a series of three subsequent tests—summation, enhancement of conditioning, and retardation—it was demonstrated that the odor had acquired active inhibitory properties. The results paralleled those obtained with more traditionally studied stimuli and techniques and hence were found to be readily predictable from a recent model of conditioning set forth by Rescorla and Wagner (1972).     

Some types of conditioned inhibitors carry collateral excitatory associations

Two experiments using summation tests in conditioned suppression with rats examined whether conditioned inhibitors generated by five different conditioning procedures have an associative structure which includes collateral excitatory associations. The existence of collateral conditioned excitation was inferred from an increase in the amount of manifest conditioned inhibition after a conditioned inhibitory stimulus (CS-) extinction treatment. The five CS-s evaluated were differential, explicitly unpaired, conditional, backward, and trace. With abbreviated conditioning (Experiment 1), the differential and explicitly unpaired CS-s exhibited conditioned inhibitory properties; the conditional, backward, and trace CS-s did not. Repeated extinction presentations of the CS- in the absence of the unconditioned stimulus unmasked conditioned inhibition to the conditional, backward, and trace CS-s revealing moderate degrees of conditioned inhibition for all five CS-s. After more extensive conditioning (Experiment 2), the explicitly unpaired and conditional CS-s were strongly inhibitory and the differential and trace CS-s were moderately inhibitory. The backward CS- was not inhibitory. Repeated presentations of the CS- in extinction unmasked conditioned inhibition to trace and backward CS-s. All five CS-s were now nearly equally inhibitory. That the measured inhibitory power of backward, trace, and conditional (after few trials) CS-s can be modulated by a CS- extinction treatment suggests that they have similar associative structures and carry, in addition to inhibitory associations, collateral excitatory associations that mask the expression of conditioned inhibition.     

Enhancement of Pavlovian conditioned inhibition achieved by posttraining inflation of the training excitor

In two conditioned lick suppression experiments using water-deprived rats, we examined the effects of following Pavlovian conditioned inhibition training (i.e., A–US/AX-NoUS) with pairings of the training excitor (A) and the unconditioned stimulus (US). Experiments 1 and 2 assessed the effects of this posttraining inflation treatment on Pavlovian conditioned inhibition using a summation test and a retardation test, respectively. Both experiments revealed that subjects exposed to inflation treatment demonstrated behavior indicative of enhanced conditioned inhibition compared to subjects that did not receive inflation treatment. The results in conjunction with other recent findings suggest that posttraining associative deflation (i.e., extinction of A) and inflation effects are more symmetrical than has previously been realized.     

Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation.

Rabbits received 0 to 450 exposures of a tone conditioned stimulus (CS) prior to classical defensive conditioning of the nicitating membrane response based on an infraorbital eye shock unconditioned stimulus. Tone preexposure resulted in retarded conditioning in normal rabbits. This latent inhibition effect was not present in animals with bilateral dorsal hippocampectomy produced by aspiration. Control animals with bilateral neocortical and callosal aspiration lesions demonstrated a latent inhibition effect similar to that shown by normal nonoperated animals. The failure of CS preexposure to retard conditioning in hippocampal rabbits was not due to differences in threshold of the conditioned response to the CS or to differences in response mechanisms as determined by tests of habituation and dishabituation of the unconditioned response. A subsequent experiment employed combined-cue summation tests to confirm the fact that preexposure did not endow the tone with conditioned as well as latent inhibitiory properties. Finally, tests of stimulus generalization along the auditory frequency dimension indicated flatter relative gradients for hippocampals than for nonoperated controls, with cortical controls in between. These findings were discussed in terms of Douglas' model of hippocampal function.     

Inhibitory conditioning resulting from a reduction in the magnitude of reinforcement

Five experiments, all employing conditioned suppression in rats, studied inhibitory conditioning to a stimulus signalling a reduction in shock intensity. Experimental subjects were conditioned to a tone signalling a 1·0 mA shock and to a tone-light compound signalling a 0·4 mA shock. On a summation test in which it alleviated the suppression maintained by a third stimulus also associated with the 1·0 mA shock, the light was established as a conditioned inhibitor. Retardation tests gave ambiguous results: the light was relatively slow to condition when paired, either alone or in conjunction with another stimulus, with the 0·4 mA shock, but the difference from a novel stimulus control group was not significant. Two final experiments found no evidence at all of inhibition on a summation test in which the light was presented in conjunction with a stimulus that had itself been associated with the 0·4 mA shock. The results of these experiments have implications for the question of what animals learn during the course of inhibitory conditioning.     

Pigeons' withdrawal from an appetitive conditioned inhibitor under two training procedures

The approach-withdrawal behaviour of pigeons to a red keylight was measured under three conditions; a negative contingency (NC) between keylight and food reinforcement, a CI or conditioned inhibition procedure where the keylight was non-reinforced in compound with a tone which was reinforced when presented alone, and a random control procedure (RC). The keylight-food contingencies in CI and NC were identical, and keylight and food presentation frequency were the same in all conditions. Subsequently the effect of adding the red keylight to a novel CS+ during or after excitatory conditioning was examined (summation test of inhibition). The inhibitory procedures, CI and NC, generally yielded similar functions for the acquisition of withdrawal, and the results of the withdrawal and summation measures were positively correlated. The implications of the results for theories of the acquisition and behavioural action of conditioned inhibitors are discussed.     

Counteraction between two kinds of conditioned inhibition training

In a Pavlovian fear-conditioning preparation, we investigated the effects of combining Pavlovian and explicitly unpaired inhibition treatments. A summation test for inhibition suggested a strong tendency toward unpaired inhibition when that treatment was administered alone and found robust Pavlovian inhibition when that treatment was administered alone, but detected little behavior indicative of inhibition in subjects that experienced both treatments during training. The retardation test showed reliable unpaired and Pavlovian inhibition when these treatments were administered alone but no indication of inhibition in subjects that experienced both treatments. These counterintuitive results suggest that in some circumstances the effects of two inhibitory treatments are not additive but rather counteractive. The present results provide some information about the nature of conditioned inhibition and, more generally, cue interaction.     

Transfer of conditioned inhibition across different aversive reinforcers in the rat

Three experiments using a conditioned suppression procedure in rats assessed transfer of conditioned inhibition across different aversive reinforcers. Experiment 1, using shock and car horn blast as reinforcers, showed that a noise negatively correlated with 0.7-mA shock between sessions attenuated suppression of lever pressing elicited by the signals for 0.7-mA shock and 110-db horn blast. Similarly, when the noise signaled the omission of horn blast, it attenuated suppression elicited by the signals for horn blast and shock. Experiment 2, using the same procedure, replicated transfer of conditioned inhibition from shock to horn found in Experiment 1, and indicated that such effects should be attributed to associative factors. Experiment 3, using the conditioned inhibition paradigm and different chambers during training and testing, replicated transfer from horn to shock and indicated that transfer cannot be attributed to multiple-background-reinforcer associations established during inhibitory training. The results of these experiments have implications for theories of conditioned inhibition.     

Extinction of an emotional response in the presence of facial expressions of emotion

Previous studies (Lanzetta & Orr, 1980, 1981; Orr & Lanzetta, 1980) have demonstrated that fear facial expressions have the functional properties of conditioned excitatory stimuli, while happy expressions behave as conditioned inhibitors of emotional responses. The present study uses a summation conditioning procedure to distinguish between associative and nonassociative (selective sensitizations, attentional) interpretations of these findings. A neutral tone was first established as a conditioned excitatory CS by reinforcing tone presentations with shock. In subsequent nonreinforced test trials the excitatory tone was paired with either fear, happy, or neutral facial expressions. A tone alone and a tone/nonface slide compound were used as controls. The results indicate that phasic and tonic skin conductance responses to the tone/fear expression compound were significantly larger during extinction than for all other experimental and control groups. No significant differences were found among these latter conditions. The findings support the assumption that the excitatory characteristics of fear expressions do not depend on associative mechanisms. In the presence of fear cues, fear facial expressions intensify the emotional reaction and disrupt extinction of a previously acquired fear response. Happy facial expressions however, do not function as conditioned inhibitors in the absence of reinforcement, suggesting that the previously found inhibition was associative in nature.This research was supported by NSF grant No. 77-08926 and by funds from the Lincoln Filene Endowment to Dartmouth College.     

Predictive learning in nutrient-based flavor conditioning

This paper presents two experiments on nutrient-based flavor conditioning with rats as subjects and sucrose as the unconditioned stimulus (US). Experiment 1 was aimed at establishing an optimal control for conditioning, comparing simultaneous and serial presentations of a flavor and the US. The results showed that simultaneous, but not serial training, produced conditioning. Experiment 2 was designed to obtain evidence of summation as an index of both conditioned inhibition and predictive learning. Group Simultaneous received Pavlovian conditioned inhibition training during which flavor A was simultaneously paired with sucrose on excitatory trials (A+), and forming an unreinforced compound with flavor B on inhibitory trials (AB-). An independent excitor for the summation test was also trained by simultaneous pairings with sucrose (C+). In the control group (Blocked), the AB- trials were presented forming a block at the beginning of training to avoid a negative contingency-relationship with sucrose, and flavor A received serial rather than simultaneous pairing with sucrose (A --> +). On the summation test, only in group Simultaneous was consumption of the CB compound lower than that of flavor C alone, suggesting that, during training, flavor A activated an expectancy of the US occurrence.     

Contextual control over conditioned responding in a latent inhibition paradigm

We used 1-, 2-, and 3-context designs to study the control exerted by contexts over freezing in rats exposed to a conditioned stimulus (CS) in advance of its pairing with a shock unconditioned stimulus. The latent inhibition observed when preexposure, conditioning, and testing occurred in the same context was attenuated if preexposure occurred in a different context to conditioning and testing. Latent inhibition (i.e., attenuated performance) was restored in a CS-specific manner if preexposure and testing occurred in the same context and conditioning in a different one. Latent inhibition was also reduced by a long retention interval but remained specific for a particular context-CS relation. Finally, CS preexposure resulted in contextual control over the expression of excitatory conditioned performance. The results are discussed in terms of memory, associative, and associative-performance models of CS-preexposure effects.     

The effects of preexposure-test and conditioning-test intervals on the magnitude of latent inhibition

Using the conditioned taste aversion paradigm, two experiments were conducted to examine the effects of the interval between preexposure and test and that between conditioning and test on the magnitude of latent inhibition. Experiment 1 revealed that the degree of latent inhibition was attenuated when rats were given a 21‐day interval between preexposure and test. It was also found that this attenuation was more marked in subjects which were given conditioning immediately after preexposure than those which were conditioned shortly before the test. Retention interval between preexposure and test was reduced to 12 days in Experiment 2, and exactly the same pattern of results as those found in Experiment 1 was obtained. These findings suggest that the memory of conditioning as well as that of preexposure decreases its retrievability after a long retention interval, although the former is more retainable than the latter.     

Suprathreshold binocular interactions for grating patterns

Binocular interactions of suprathreshold grating patterns have been investigated using a reaction time measure of contrast detection. Simple reaction times were determined for monocular and binocular viewing conditions over a contrast range from .63 to near threshold. The results from all subjects showed binocular summation for contrast levels near threshold, but there was considerable variation across subjects for contrast levels above threshold. Some subjects showed summation over the entire contrast range, but other subjects showed either binocular inhibition or binocular facilitation for some range of contrast levels. The pattern of binocular interaction for a given subject was consistent for several spatial frequencies. The differences in types of interaction between subjects, the variation in magnitude of binocular interaction with contrast level for each subject, and the data from experiments involving stimulation of noncorresponding retinal areas show that the binocular interactions found for suprathreshold stimuli cannot be accounted for on the basis of probability, and must, therefore, result from physiological interactions between the two eyes. These interactions have been investigated further under conditions of (1) induced fixation disparity, (2) horizontal gratings, and (3) orthogonally oriented gratings.