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.     

Context Specificity of Excitation and Inhibition in Ambiguous Stimuli

Two experiments examined the susceptibility of excitation and inhibition to contextual change when the conditioned stimulus (CS) was ambiguous using an appetitive conditioning paradigm. In Experiment 1, excitation to a CS was lost with a context switch when inhibition had been learned to the CS in a prior feature-negative (FN) discrimination. Control groups that had received either more or less excitatory conditioning in the absence of inhibitory pretraining showed no loss. In Experiment 2 inhibition was lost with a context switch in a group that had received excitatory and then inhibitory conditioning with the CS. No loss was observed in a group that had not received excitatory pretraining. The results suggest that contexts are especially likely to control performance to ambiguous CSs when they can modulate the second of two learned associations. Results are discussed in terms of their implications for occasion setting and modern conditioning theory.     

Second-order conditioning of Pavlovian conditioned inhibition

Two experiments are reported which investigated the conditioning of inhibition to a neutral stimulus as a result of its repeated pairing with a previouslyconditioned inhibitor. Both experiments employed a conditioned suppression technique with rat subjects. Experiment 1 detected the second-order inhibition through the retarded acquisition of concurrently administered excitatory conditioning. Experiment 2 found similar retardation in the acquisition of excitatory fear conditioning following previous second-order conditioning of inhibition to the stimulus. Implications are discussed for theories of the nature of inhibition and for second-order conditioning as an assessment technique.     

Spontaneous recovery of excitation but not inhibition

Five magazine approach experiments with rats and 1 sign-tracking experiment with pigeons explored the possibility of an analogue to spontaneous recovery of excitatory conditioning from extinction: spontaneous recovery of inhibitory conditioning from training. Stimuli were 1st treated as conditioned inhibitors and then as conditioned exciters or as irrelevant to reinforcement. At issue was whether the passage of time after the 2nd treatment would allow partial restoration of the initial conditioned inhibition. The experiments differed in the design used to study recovery, the manner of reinforcing the inhibitor, the means of testing for recovery, the time interval allowed for recovery, and the species used. None of the experiments found evidence for recovery of the inhibitory learning with time, despite the concurrently measured presence of spontaneous recovery of excitatory conditioning after extinction. These experiments suggest that changes with time may be preferential to the learning that occurs during extinction.     

Pavlovian conditioned inhibition of fear during shuttlebox avoidance behavior

Three experiments explored the development and function of conditioned inhibition of fear during the acquisition and maintenance of shuttlebox avoidance behavior. The development of inhibition to an exteroceptive feedback stimulus was found to be a function of the number of successive avoidance responses to which the animal had been trained and of the duration of the intertrial interval, a parameter shown also to affect the rate of acquisition of avoidance learning. Master animals who learned the instrumental avoidance response, and yoked animals who did not, showed equivalent inhibitory fear conditioning in each experiment. The results of one experiment suggest that conditioned inhibition plays no important role in “protecting” fear conditioned to the discrete warning signal during avoidance maintenance. These data indicate that feedback stimuli develop their inhibitory properties by a Pavlovian process and that certain aspects of their function may, therefore, be readily understood within the framework of mediational two-process learning theory.     

Mechanisms underlying retarded emergence of conditioned responding following inhibitory training: evidence for the comparator hypothesis

The comparator hypothesis posits that conditioned responding is determined by a comparison at the time of testing between the associative strengths of the conditioned stimulus (CS) and stimuli proximal to the CS at the time of conditioning. The hypothesis treats all associations as being excitatory and treats conditioned inhibition as the behavioral consequence of a CS that is less excitatory than its comparator stimuli. Conditioned lick suppression by rats was used to differentiate four possible sources of retarded responding to an inhibitory CS. These include habituation to the unconditioned stimulus (US), latent inhibition to the CS, blocking of the CS-US association by the conditioning context, and enhanced excitatory associations to the comparator stimuli. Prior research has demonstrated the first three phenomena. Therefore, we employed parameters expected to highlight the fourth one--the comparator process. In Experiment 1, our negative contingency training was shown to produce a conditioned inhibitor that passed inhibitory summation and retardation tests. In Experiment 2 we found transfer of retardation from an inhibitory CS to a novel stimulus when the location where retardation-test training occurred was excitatory, which is indicative of contextual blocking and/or comparator effects. In Experiment 3, extinction of the conditioning context was found to attenuate retardation regardless of whether extinction occurred before or after the CS-US pairings of the retardation test. This indicates that much of the present retardation was due to the comparator process rather than to contextual blocking. Experiment 4 demonstrated that habituation to the US did not contribute to retardation in the present case. Collectively, these studies suggest that retardation following inhibitory training can be explained without recourse to any of the traditional mechanisms of conditioned inhibition.     

Stimulus generalization of excitation and inhibition

Five sign-tracking experiments with pigeons investigated the breadth of stimulus generalization of excitatory and inhibitory conditioning. Using a compound stimulus test procedure, these experiments found evidence for a narrower generalization of associative strength in excitation than in inhibition. They also found a narrower associative gradient with a more strongly conditioned excitatory stimulus, although this did not seem to account for the difference between exciters and inhibitors. These results confirm earlier findings comparing generalization after acquisition and extinction and raise various theoretical issues about generalization.     

Stimulus generalization of excitation and inhibition

Five sign-tracking experiments with pigeons investigated the breadth of stimulus generalization of excitatory and inhibitory conditioning. Using a compound stimulus test procedure, these experiments found evidence for a narrower generalization of associative strength in excitation than in inhibition. They also found a narrower associative gradient with a more strongly conditioned excitatory stimulus, although this did not seem to account for the difference between exciters and inhibitors. These results confirm earlier findings comparing generalization after acquisition and extinction and raise various theoretical issues about generalization.     

Contextual Control of Latent Inhibition by the Reinforcer

Three experiments examined the contextual control of latent inhibition (LI) by the unconditioned stimulus (US) using a within-subjects conditioned suppression procedure with rats. The effect of reducing the context change produced by the introduction of the shock US was investigated by presenting this US during preexposure to the conditioned stimulus (CS). Although limited CS preexposure in the absence of the US had no impact on subsequent conditioning, preexposure in the presence of the shock retarded both excitatory and inhibitory conditioning. We conclude that the introduction of the US during the conditioning phase of a normal LI experiment can produce a contextual change that reduces the observed magnitude of LI.     

Contralateral transfer of inhibitory and excitatory eyelid conditioning in the rabbit

In Experiment I, rabbits received training to establish a clicker as a conditioned inhibitor. In a subsequent test phase this stimulus was used as a signal for shock either to the eye reinforced during initial training or to the opposite eye. Learning to the clicker was slower in both conditions than in the appropriate control groups. The second experiment replicated the results of those subjects trained and tested with opposite eyes and ruled out the possibility that the slower learning was due to the effects of latent inhibition. Experiment III demonstrated that excitatory conditioning to a clicker to one eye facilitated future excitatory conditioning to that stimulus to the opposite eye. These results are consistent with the view that inhibitory and excitatory conditioning both involve the acquisition of a general, motivational conditioned response which is capable of mediating the transfer of conditioning across different response systems.     

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.     

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.     

Conditioning across the duration of a backward conditioned stimulus

Five conditioned suppression experiments examined the extent to which an appetitively motivated lever-press response can be punished by different components of a backward conditioned stimulus (CS). Using a 0-s unconditioned stimulus (US)-CS interval, Experiments 1 and 2 showed that the initial 3 s of a normally 30-s backward CS served as a more effective punisher than the CS as a whole. Experiment 3 found no such effect if the US-CS interval were 3 s rather than 0 s. Experiments 4A and 4B found that if the US-CS interval were 0 s, the initial part of the backward CS acquired excitatory properties although the CS as a whole passed a summation test for conditioned inhibition. By contrast, the 3-s US-CS interval supported inhibitory conditioning across the whole duration of the backward CS. Taken together, these findings support a modified version of Wagner's sometimes opponent process model, which suggests that different components of a backward CS become either excitatory or inhibitory depending on the components' temporal proximity to the US.     

Distractor effect on the latent inhibition of conditioned flavor aversion in rats

Using a conditioned flavor aversion procedure with rats as subjects, the effect of the addition of a distractor stimulus on the magnitude of the latent inhibition effect was examined. Experiment 1 showed that latent inhibition to vinegar was attenuated by the addition of sucrose during preexposure. On the other hand, sucrose added during conditioning to vinegar did not attenuate latent inhibition. It was also found that the degree of latent inhibition to the vinegar-sucrose compound solution was less when vinegar alone was preexposed (i.e., when sucrose was added only during conditioning) than when the compound solution was preexposed (i.e., when sucrose was added both during preexposure and during conditioning). Experiment 2 gave similar results but with sucrose assigned as the target flavor and vinegar as the distractor. These findings are in full agreement with the generalization decrement account of latent inhibition.     

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.     

Superconditioning from a reduced reinforcer

In four autoshaping experiments pigeons received conditioned inhibition training of the form A++, AB-, where ++ is a strong reinforcer and - is nonreinforcement. Subsequent AB+ training, in which + is a moderate reinforcer, resulted in enhanced conditioning of A, relative to an A stimulus receiving no treatment, one receiving A+ treatment, and one receiving A++ treatment. This enhancement of conditioning to Aconstitutes a demonstration of “superconditioning”. The presence of the inhibitory B sufficiently enhanced the reinforcing power of the moderate reinforcer (+) that it was able to further increase the excitation controlled by A. This occurred even though A had previously been paired with a stronger reinforcer (++). Superconditioning was also observed when A and B were extinguished prior to treatment with + or were originally neutral stimuli followed by + in the presence of an inhibitor trained elsewhere.     

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.     

The comparator hypothesis of conditioned response generation: manifest conditioned excitation and inhibition as a function of relative excitatory strengths of CS and conditioning context at the time of testing

In the present research water-deprived rats were used in a conditioned lick suppression paradigm to test and further develop Rescorla's (1968) contingency theory, which posits that excitatory associations are formed when a conditioned stimulus (CS) signals an increase in unconditioned stimulus (US) likelihood and that inhibitory associations develop when the CS signals a decrease in US likelihood. In Experiment 1 we found that responding to a CS varied inversely with the associative status of the context in which the CS was trained and that this response was unaltered when testing occurred in a distinctively dissimilar context with a different conditioning history, provided associative summation with the test context was minimized. These results suggest that manifest excitatory and inhibitory conditioned responding is modulated by the associative value of the training context rather than that of the test context. In Experiment 2 it was demonstrated that postconditioning decreases in the associative value of the CS training context reduced the effective inhibitory value of the CS even when testing occurred outside of the training context. Moreover, this contextual deflation effect was specific to the CS training context as opposed to any other excitatory context. Collectively, these studies support the comparator hypothesis, which states that conditioned responding is determined by a comparison of the associative strengths of the CS and its training context that occurs at the time of testing rather than at the time of conditioning. This implies that all associations are excitatory and that responding indicative of conditioned inhibition reflects a CS-US association that is below (or near) the associative strength of its comparator stimulus. It is suggested that response rules which go beyond a monotonic relation between associative value and response strength can partially relieve learning theories of their explanatory burdens, thereby allowing for simpler models of acquisition.     

Testing response generation rules

Robbins (1988) reported data that he viewed as inconsistent with Miller and Schachtman's (1985a) comparator hypothesis of conditioned response generation. Here we explain why we do not find his experiments a compelling test of the comparator hypothesis. We also briefly review other studies that tested the same predictions of the comparator hypothesis that Robbins examined. We conclude that there is considerable evidence that following excitatory or inhibitory conditioning with a target conditioned stimulus (CS) and unconditioned stimulus (US), extinction of other cues that were present during CS training ordinarily increases excitatory responding and decreases inhibitory responding to the CS. However, consistent with Robbins's conclusion, there is scant evidence that after CS-US training, enhancing the associative value of other cues that were present during CS training influences excitatory or inhibitory responding to the CS. The implications of these conclusions for the comparator hypothesis as an explanation of differences in acquired behavior and as a heuristic tool are considered.     

Comparing excitatory backward and forward conditioning

Three Pavlovian lick suppression studies with rats were conducted to compare the role of the conditioning context in excitatory backward and forward conditioning. The experiments explored the possibility that excitatory backward conditioning, but not forward conditioning, is mediated by the context. That is, in excitatory backward conditioning, the conditioning context may function as an excitatory mediator, which supports second-order conditioning of the target cue. This possibility contrasts with traditional accounts, which suggests that common processes underlie excitatory backward and forward conditioning. Experiment 1 found that conditioned responding following backward conditioning was attenuated as a result of posttraining extinction of the training context, but the same manipulation elevated responding after forward conditioning. Experiments 2 and 3 found that posttraining and pretraining associative inflation of the context (presenting unsignalled USs) increased conditioned responding to the target of a backward conditioning procedure but either had no effect or reduced responding to the target of a forward conditioning procedure. Thus, excitatory backward and forward conditioning appear to differ in their dependence on the status of the conditioning context.