Directed approach responses and positive conditioned suppression in the rat

Three experiments evaluated an alternative to accounts of positive conditioned suppression that stress central (i.e., motivational or emotional) states. This “competing-response” interpretation was tested by analyzing directed movements that develop in rats during a visual or an auditory stimulus (CS) that signals an appetitive reinforcer (US) in a situation where the subject is also emitting an instrumental response for food. In each experiment, positive conditioned suppression (i.e., a reduction in the rate of such instrumental responding during CS presentations) was accompanied by responses directed toward the CS source and/or the US-delivery site. In Experiment 1, a diffuse (auditory) CS signaled a US delivered at some specific place in the chamber and rats approached the US-delivery site during CS. In Experiments 2 and 3, the spatial proximity of a localized visual CS and US-delivery site determined whether CS-directed or US-directed behavior predominated during the CS. The results suggest that the topographies of conditioned responses on any positive conditioned suppression procedure depend upon the spatial arrangements of features that elicit and support these behaviors. They further suggest that the identification of these features and their spatial arrangements is necessary for the analysis of appetitive classical-instrumental interactions.     

Context sensitivity of conditioned suppression following preexposure to the conditioned stimulus

Conditioned suppression in rats is often unaffected when the context (or set of background stimuli) is changed following conditioning. This suggests that responding to the conditioned stimulus (CS) can be relatively insensitive to the context in which the CS is presented. In two experiments, we examined whether sensitivity to contextual stimuli is affected by preexposure to the CS. In Experiment 1, when the CS was novel at the outset of conditioning, conditioned suppression was not affected when the context was changed following conditioning. However, when the CS had been preexposed, responding was weaker when extinction occurred outside of the conditioning context. In Experiment 2, responding was again sensitive to the test context, regardless of whether preexposure occurred in the conditioning context or in an alternate context. These results suggest that the extent to which responding is sensitive to context can depend on the conditioning history of the CS.     

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.     

Conditioned suppression of a positively reinforced shuttle response

Rats were trained to run up and down an alleyway for sucrose reinforcement on a variable interval schedule. Differential aversive classical conditioning with auditory CSs was then conducted in a separate apparatus (“off the baseline”) prior to those CSs being presented while the subjects were responding for sucrose in the alleyway. Once the effects of the CSs had extinguished, shock was reintroduced following one CS but not the other (“on the baseline” differential aversive classical conditioning). Both “off the baseline” and “on the baseline” conditioning resulted in conditioned suppression to the CS followed by shock, but little effect of the CS followed by no shock was found. In the “on the baseline” phase, total suppression of baseline responding occurred at moderate US intensities, and this appeared to result from the subject avoiding the location at which he was last shocked. At lower values, both baseline response rate and relative suppression ratio were functions of US intensity. The results are discussed in relation to the effects found in similar experiments using avoidance baselines.     

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.     

Omission training and positive conditioned suppression in the rat

Suppression of operant responding during a conditioned stimulus (CS) was studied in two procedures. In both procedures, operant leverpressing was maintained by a variable-interval 1-min food-delivery schedule, and insertion of a second lever served as the CS. In the first procedure, autoshaping, food followed each CS presentation irrespective of a subject’s behavior during the CS. In the second procedure, omission training, contact with the CS canceled the delivery of food scheduled for the end of that CS. In the first experiment, subjects were exposed to omission training followed by autoshaping; these procedures were reversed in the second experiment. In each experiment, the omission contingency resulted in fewer CS contacts and less suppression of operant responding during the CS than did autoshaping. These differences were more notable in subjects receiving the sequence autoshaping→omission training (Experiment 2). Direct observations in Experiment 2 revealed that, for subjects that were contacting the CS frequently when the omission contingency was introduced, reductions in signal contacts were accompanied by redistributions of behavior. The form of these redistributions depended upon behavior allocation at the time the omission contingency was imposed.     

Stepwise reductions in US density and intensity: Maintenance and extinction of conditioned suppression

Information was sought on how the strength of fear, acquired and extinguished in a classical conditioning paradigm, might be affected by certain of the circumstances that normally are associated with the course of avoidance learning. Following preconditioning exposures to the conditioned stimulus, one group of rats (Group PRF) was given continuous conditioned stimulus-unconditioned stimulus (CS-US) acquisition trials followed by stepwise reductions in US probability (given the CS) over three phases to about 11% for the final phase. Another group, Group US(lo), was given continuous CS-US pairings throughout, but, following acquisition, received stepwise reductions in US intensity (to permit evaluation of a progressively changing feature of the US over a wide range without having to employ excessive shock) over the same phases. A third group, Group US(hi), received unchanging (from acquisition) CS-US pairings over these phases, and an explicitly unpaired control group (Group RU) was included. Although outcomes differed somewhat depending upon whether suppression ratios or absolute measures of responding were considered, the major findings were that suppression to the CS was complete by the end of acquisition and persisted thereafter throughout the three phases for all but control subjects. In contrast to Group US(lo), which showed relatively little resistance to extinction of suppression to subsequent CS-only exposures, Groups US(hi) and PRF displayed marked resistance over two separate, extended sets of extinction sessions. Suppression to context cues was pronounced only for Groups US(hi) and RU, and varied as a function of US parameters and not whether the shocks were or were not signaled. Theoretical reconciliation of these findings was most difficult for Groun PRF.     

Transfer of conditioned suppression and conditioned acceleration from instrumental to consummatory baselines

Following training on a variable-interval food reinforcement schedule, rats were exposed to Pavlovian procedures which produced reliable conditioned suppression and conditioned acceleration of the leverpressing (instrumental) baseline. When free food was simultaneously made available in the test cage, all subjects spent the majority of each session “freeloading,” that is, eating food from a dish rather than leverpressing for it. When superimposed upon the freeloading baseline, the conditioned suppression and conditioned acceleration procedures affected the rate of pellet consumption identically in magnitude and direction to their previous effects on leverpressing. These results suggest a motivational mechanism for conditioned suppression and acceleration, rather than one which depends upon spurious punishment of specific response sequences.     

A test of two methods for extinguishing Pavlovian conditioned inhibition

Two experiments were performed using rats in a conditioned suppression procedure to test two different methods for extinguishing Pavlovian conditioned inhibition. In both experiments, a target stimulus, X, was made inhibitory by giving discrimination training of the form A+ AX?. Then, in Experiment 1, an attempt was made to extinguish the inhibition conditioned to X by presenting nonreinforced occurrences of X, of AX, and of A. Testing for conditioned inhibition took the form B+ BX?. It was found that the extinction procedure did not weaken the inhibitory properties of X. Experiment 2 attempted to extinguish the inhibition conditioned to X by presenting X randomly and independently of the reinforcer, electric grid shock. This procedure appeared to weaken inhibition quickly and permanently.     

Acquired equivalence and generalized suppression in a virtual reality environment

Acquired equivalence was investigated using a virtual reality conditioned suppression task administered in a first-person-shooter game. Two visual cues, A1 and B1, were followed by a tone (O1), and another two cues, A2 and B2, were followed by another tone (O2). During differential Pavlovian conditioning, A1 was paired with an instructed unconditioned stimulus (US) consisting of a flashing white screen, whereas A2 was not. All cues and outcomes were then presented at test, in the absence of the US, and suppression ratios were calculated for multiple response topographies (shots, hits, and breaks). Clear evidence of the suppression of shots was seen for A1 and B1, with no suppression being seen for either A2 or B2. Presentations of O1 and O2 resulted in significant suppression of shots and hits, whereas only O1 led to the suppression of breaks. The US expectancy ratings were consistent with these behavioral results. The findings are discussed in the light of differing accounts of acquired equivalence.     

A concurrent assessment of the positive and negative properties of a signaled shock schedule

A choice and a conditioned suppression procedure were used to assess concurrently the positive and negative properties of stimuli within a signaled shock schedule, Occasional shocks were presented to Ss responding on a variable-interval food schedule. Ss could choose whether shocks occurred alone or whether they were preceded by a 1-min signal. All Ss chose the signaled shock condition over the unsignaled one, even though food reinforced responding in the presence of the signal was suppressed. Rate of responding for food varied across stimulus conditions, with the lowest rate in the presence of the signal and the highest rate in its absence. An intermediate rate occurred under the unsignaled shock schedule. A safety analysis was applied to the data.     

Procedure and reliability of conditioned respiratory suppression

Changes in respiration amplitude, respiration rate, and heart rate in response to a conditioned signal for shock were measured concurrently in kittens and adult cats. The data were analyzed with respect to qualitative and quantitative variability across trials and subjects; correlation among measures; skewness; and kurtosis. Suppression of respiration amplitude was the most reliable response across trials and subjects, with increases in respiration rate second and heart rate by far the least reliable. Correlations between each pair of measures were moderate. Respiration-amplitude responses were negatively skewed, but this deviation from normality was moderate and consistent across subjects. The measurement of conditioned respiratory suppression is a viable addition or alternative to the conditioned emotional response procedure in studies of classically conditioned fear.     

Effects of a backward conditioning procedure following acquisition on extinction of conditioned suppression

A one-trial-a-day procedure was used to investigate the effects of US-CS pairings on extinction of conditioned suppression of licking by rats. Following acquisition trials, response suppression was immediately eliminated when US preceded CS, but it reappeared during subsequent CS-alone presentations. Ss that received backward pairings reached a significant level of extinction one trial before Ss that received conventional extinction trials.     

Renewal of Pavlovian conditioned inhibition

Prior research has demonstrated renewal, which is the ability of contextual cues to modulate excitatory responding to a Pavlovian conditioned stimulus (CS). In the present research, conditioned lick suppression in rats was used to examine similar contextual modulation of Pavlovian conditioned inhibition. After Pavlovian conditioned inhibition training with a CS in one context, subjects were exposed to pairings of the CS with an unconditioned stimulus (US) either in the same or in a second context. Results indicated that, when the CS was paired with the US in the second context, the CS retained its inhibitory control over behavior, provided that testing occurred in the context used for inhibition training. However, when the CS-US pairings occurred in the inhibition training context, the CS subsequently proved to be excitatory regardless of where testing occurred. These observations indicate that conditioned inhibition is subject to renewal.     

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.     

Conditioned inhibition training of the competing cue after compound conditioning does not reduce cue competition

In each of two experiments, we studied Pavlovian fear conditioning (as assessed by barpress conditioned suppression) in 32 albino rats. Following a two-stage cue-competition procedure (A+ then AX+), we subjected the competing cue (A) to conditioned inhibition training (B+, BA?) before testing the target cue (X). Conditioned inhibition training was designed to weaken the putative A-unconditioned stimulus (US) association, perhaps changing it to an A-no-US association. Performance-deficit theories of cue competition, such as comparator theory and retrieval-interference theory, predict that such procedures should weaken cue competition, causing Conditioned Stimulus X (CS X) to evoke strong responding. The same prediction can be deduced from recent acquisition-focused models (Dickinson &; Burke, 1996; Van Hamme &; Wasserman, 1994). In opposition to this prediction, however, we found in both experiments that conditioned inhibition training had no detectable effect on cue competition even though it successfully abolished conditioned responding to CS A. In Experiment 2, moreover, we found evidence against the hypothesis that the weak response to CS X was due to generalization decrement rather than to cue competition. Results favor early learning-deficit theories of cue competition over performance-deficit theories and over the recent acquisition-focused models.     

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

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

Conditioned suppression is an inverted-U function of footshock intensity

Most theories of associative learning assert that conditioned responding to a target cue is a monotonically increasing function of unconditioned-stimulus (US) intensity. In a lick suppression preparation with rats, a cue was paired with a 0.4-, 0.6-, 0.8-, 1.0-, 1.2-, or 1.4-mA footshock in Experiment 1a, and with a 0.3-, 0.8-, 1.3-, or 1.8-mA footshock in Experiment 1b. Subsequent suppression in response to the cue was an inverted-U function of the US intensity. In Experiment 2, we demonstrated that massive extinction of the training context and compound conditioning can each attenuate the response decrement caused by training with a high-intensity US. The sometimes-competing-retrieval model (Stout & Miller, Psychological Review 114:759–783, 2007) provides a better fit to these data than do several other models of associative learning.     

Temporal encoding in trace conditioning

Conditioned lick suppression in rats was used to explore the role of timing in trace conditioning. In Experiment 1, two groups of rats were exposed to pairings of a CS (CS1) with a US, under conditions in which the interstimulus interval (ISI) that separated CS1 offset and US onset was either 0 or 5 sec. Two additional groups were also exposed to the same CS1→US pairings with either a 0 or a 5-sec ISI, and then received “backward” second-order conditioning in which CS1 was immediately followed by a novel CS2 (i.e., CS1→CS2). A trace conditioning deficit was observed in that the CS1 conditioned with the 5-sec gap supported less excitatory responding than the CS1 conditioned with the 0-sec gap. However, CS2 elicited more conditioned responding in the group trained with the 5-sec CS1-US gap than in the group trained with the 0-sec CS1-US gap. Thus, the CS1-US interval had inverse effects on first- and second-order conditioned responding. Experiment 2 was conducted as a sensory preconditioning analogue to Experiment 1. In Experiment 2, rats received the CS1?CS2 pairings prior to the CS1→US pairings (in which CS1 was again conditioned with either a 0 or a 5-sec ISI). Experiment 2 showed a dissociation between first- and second-order conditioned responding similar to that observed in Experiment 1. These outcomes are not compatible with the view that differences in responding to CSs conditioned with different ISIs are mediated exclusively by differences in associative value. The results are discussed in the framework of the temporal coding hypothesis, according to which temporal relationships between events are encoded in elementary associations.     

One-trial simultaneous and backward excitatory fear conditioning in rats: Lick suppression, freezing, and rearing to CS compounds and their elements

Three experiments with rat subjects sought to enhance one-trial excitatory simultaneous and backward fear conditioning by using a two-element compound conditioned stimulus (CS) instead of only a single element. During conditioning, experimental groups received a 4-sec CS either coextensively with a 1-mA grid-shock unconditioned stimulus (US) or immediately after US termination. In subsequent tests, CSs evoked more lick suppression and freezing in these groups than in various controls. Compound CSs evoked more lick suppression and freezing than did CS elements, but did so equally for experimental and control groups. Therefore, the use of compounds did not enhance conditioning. Unexpectedly, an explicitly unpaired control in which CS followed US termination by 3 min tended to show more CS-evoked suppression and freezing than did a control in which CS preceded US onset by 3 min. This result raises the possibility that associations between the CS and the training context might engender responding to backward-paired CSs.