Reexamination of contextual conditioning with massed versus distributed unconditioned stimuli

Sprague-Dawley rats were placed in the black compartment of a 2 compartment choice apparatus and received a series of unsignaled footshocks at fixed intertrial intervals (ITIs), with ITI duration varied across groups. Contextual conditioning was assessed using place preference and freezing tests. In Experiments 1 and 3, time spent in the unshocked, white compartment in a preference test decreased monotonically with increasing ITI. In Experiment 2, less freezing occurred in the 3-s than in the 60-s groups. An inverted U-shaped relationship between ITI and freezing emerged when a full range of ITIs was used in Experiment 3. The results have implications for the learning-performance distinction and suggest that short ITIs may promote contextual conditioning.     

Pavlovian conditioning with proximal stimuli

This experiment was conducted with the objective of demonstrating that the effective stimuli in Pavlovian Conditioning are not environmental stimuli but internal physiological processes elicited by environmental input (proximal stimuli). In order to achieve the objective, afterimages in color vision were used: looking at a diffuse lightened circle after seeing a red circle yields an image of a green circle. A differential conditioning paradigm with two sequential compounds was run. In one group (G⁺B^?: n₁=10), a red circle followed by a green circle was paired with shock, whereas a red circle followed by a blue circle remained unpaired. A second group (G^?B⁺: n₂=10) received red-blue paired trials and unpaired red-green trials. Immediately after that training, subjects were tested with a new, never trained sequential compound: a red circle followed by a diffuse lightened circle. Furthermore, they were tested with the already trained compounds. Taking the environmental point of view, the never trained stimulus should elicit an orienting response lying inbetween the excitatory reaction to the paired stimulus and the inhibitory reaction to the unpaired stimulus. From the proximal point of view, the diffuse light should elicit an excitatory reaction in group G⁺B^? and an inhibitory reaction in group G^?B⁺. Electrodermal conditioned anticipatory and omission responses were measured. The results supported the proximal hypothesis. Hence, defining input in environmental terms may be the wrong way. Instead, in conceptualizing the stimulus in conditioning, the following should be considered: the processing organism itself is creating the effective stimuli.     

Reinforcement and the organization of behavior in golden hamsters: Pavlovian conditioning with food and shock unconditioned stimuli

The effects of Pavlovian conditioned stimuli (CSs) for food or shock on a variety of behaviors of golden hamsters were observed in three experiments. The aim was to see whether previously reported differences among the behaviors produced by food reinforcement and punishment procedures could be accounted for by differential effects of Pavlovian conditioning on the behaviors. There was some correspondence between the behaviors observed to the CSs and the previously reported effects of instrumental training. However, the Pavlovian conditioned responses (CRs) alone would not have predicted the effects of instrumental training. Moreover, CRs depended to some extent on the context in which training and testing occurred. These findings, together with others in the literature, suggest that the results of Pavlovian conditioning procedures may not unambiguously predict what system of behaviors will be most readily modified by instrumental training with a given reinforcer.     

The amygdala is not necessary for unconditioned stimulus inflation after Pavlovian fear conditioning in rats

The basolateral complex (BLA) and central nucleus (CEA) of the amygdala play critical roles in associative learning, including Pavlovian conditioning. However, the precise role for these structures in Pavlovian conditioning is not clear. Recent work in appetitive conditioning paradigms suggests that the amygdala, particularly the BLA, has an important role in representing the value of the unconditioned stimulus (US). It is not known whether the amygdala performs such a function in aversive paradigms, such as Pavlovian fear conditioning in rats. To address this issue, Experiments 1 and 2 used temporary pharmacological inactivation of the amygdala prior to a US inflation procedure to assess its role in revaluing shock USs after either overtraining (Experiment 1) or limited training (Experiment 2), respectively. Inactivation of the BLA or CEA during the inflation session did not affect subsequent increases in conditioned freezing observed to either the tone conditioned stimulus (CS) or the conditioning context in either experiment. In Experiment 3, NBQX infusions into the BLA impaired the acquisition of auditory fear conditioning with an inflation-magnitude US, indicating that the amygdala is required for associative learning with intense USs. Together, these results suggest that the amygdala is not required for revaluing an aversive US despite being required for the acquisition of fear to that US.Pavlovian fear conditioning in rats is a behavioral model used to investigate the neurobiology underlying the development and maintenance of fear learning and memory (Grillon et al. 1996; LeDoux 1998, 2000; Bouton et al. 2001; Maren 2001b, 2005; Kim and Jung 2006). In this model, an innocuous conditioned stimulus (CS), such as a tone, is paired with an aversive unconditioned stimulus (US), such as a footshock. After one or more pairings, the rat learns that the CS predicts the US. As a consequence, CS presentations alone elicit a conditioned fear response (CR), which includes increases in heart rate, arterial blood pressure, hypoalgesia, potentiated acoustic startle, stress hormone release, and freezing (somatomotor immobility).The amygdala has been identified as one of the major regions in which fear memories are encoded and stored. Within the amygdala, the basolateral complex of the amygdala (BLA; consisting of the lateral, basolateral, and basomedial nuclei) and the central nucleus of the amygdala (CEA) receive convergent CS and US information and are involved in the acquisition of fear memories (LeDoux 1998, 2000; Fendt and Fanselow 1999; Davis and Whalen 2001; Maren 2001b; Schafe et al. 2001; Fanselow and Gale 2003; Wilensky et al. 2006; Zimmerman et al. 2007). In addition, the CEA has an important role in the expression of fear CRs (Fendt and Fanselow 1999; LeDoux 2000; Davis and Whalen 2001; Maren 2001b; Fanselow and Gale 2003). In support of this, many studies have shown that either permanent or temporary lesions of the BLA or CEA prevent the acquisition and/or expression of fear memories (Helmstetter 1992; Helmstetter and Bellgowan 1994; Campeau and Davis 1995; Maren et al. 1996a,b; Killcross et al. 1997; Muller et al. 1997; Walker and Davis 1997; Cousens and Otto 1998; Maren 1998, 1999, 2001a,b; Wilensky et al. 1999, 2000, 2006; Goosens and Maren 2001, 2003; Nader et al. 2001; Fanselow and Gale 2003; Gale et al. 2004; Koo et al. 2004; Zimmerman et al. 2007).In addition to its role in encoding CS–US associations during conditioning, recent work suggests that the amygdala is also involved in representing properties of the US itself. For example, temporary or permanent lesions of the BLA reduce both decrements in conditioned responding after devaluation of a food US (Hatfield et al. 1996; Killcross et al. 1997; Blundell et al. 2001; Balleine et al. 2003; Everitt et al. 2003; Pickens et al. 2003; Holland 2004) and increments in conditional responding after inflation of a shock US (Fanselow and Gale 2003). Moreover, recent electrophysiological studies in primates indicate that amygdala neurons represent the value of both aversive and appetitive outcomes (Paton et al. 2006; Belova et al. 2007, 2008; Salzman et al. 2007). These studies suggest that one function of the BLA is to represent specific properties of biologically significant events, such as the food or shock USs that are typically used in Pavlovian conditioning paradigms. By this view, the BLA may represent specific sensory properties of USs that shape the nature of learned behavioral responses to the US (Balleine and Killcross 2006) and allow CSs to gain access to the incentive value of the US (Everitt et al. 2003).In contrast to this view, we recently reported that rats with neurotoxic BLA lesions exhibit normal US revaluation after Pavlovian fear conditioning (Rabinak and Maren 2008). In this study, auditory fear conditioning (75 CS–US trials) with a moderate footshock (1 mA) was followed by several exposures (five US-alone trials) to an intense footshock (3 mA) during an inflation session. Both intact rats and rats with BLA lesions exhibit a robust increase in conditional freezing to the auditory CS during a subsequent retention test (Rabinak and Maren 2008). Control experiments suggested that this was due to a revaluation of the US with which the CS was associated, rather than nonassociative sensitization of fear engendered by exposure to intense shock. These data reveal that the BLA may not be necessary for representing properties of shock USs during Pavlovian fear conditioning. To address these issues further, we have examined the consequence of reversible pharmacological manipulations of the amygdala during US inflation on conditional fear responses established with either extensive or limited training.     

Evaluative conditioning in the picture-picture paradigm with random assignment of conditioned stimuli to unconditioned stimuli

Human participants were allocated to 1 of 3 groups. In the conditioning group, each conditioned stimulus (CS)-unconditioned stimulus (US) pair was presented 7 times during the acquisition phase. Participants who were assigned to the extinction group saw 5 additional presentations of each CS in isolation after the 7 presentations of each CS-US pair. In the latent inhibition group, the CS-only trials were presented before the CS-US trials. Overall, a significant evaluative conditioning effect was observed. This effect cannot be dismissed on the basis of the arguments developed by A. P. Field and G. C. L. Davey (1997, 1998, 1999), and the results thus provide strong evidence for the associative nature of evaluative conditioning. The results are also in line with other findings, which showed that evaluative conditioning is resistant to extinction.     

Differential effects of two ways of devaluing the unconditioned stimulus after Pavlovian appetitive conditioning

Three experiments with rat subjects investigated the effects of two methods of devaluing a food unconditioned stimulus (US) after pairings of an auditory conditioned stimulus (CS) with that US. Experiment 1 found no effect of postconditioning pairings of the food US with lithium chloride (LiCl) on general activity to a tone CS, even though those pairings substantially reduced food consumption. Experiments 2 and 3 compared the effects on conditioned responding of postconditioning pairings of food with LiCl and with high-speed rotation. In these experiments the general activity measure was supplemented by a detailed visual analysis of the rats' behavior. Experiment 2 found that food-rotation pairings had larger effects than food-LiCl pairings on general activity responding and on two detailed behavioral measures but that food-LiCl pairings had larger effects on food consumption and on one behavioral measure. Experiment 3 replicated the findings of Experiment 2 and found that the ability of the CS to serve as a reinforcer for second-order conditioning after US devaluation was reduced more by food-LiCl pairings.     

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.     

Evaluative conditioning without directly experienced pairings of the conditioned and the unconditioned stimuli

Evaluative conditioning (EC) is the valence change of a stimulus (conditioned stimulus, CS) that is due to the previous pairing with another stimulus (unconditioned stimulus, US). We investigated whether EC can occur also when the CS-US pairings are not experienced directly by the participant but are implied by other events that the participant encounters. In two experiments, positive USs were presented in some trials and negative USs in other trials. Afterwards, participants were given information from which it was possible to conclude that CSs were covertly present during these trials. Finally, the valence of these CSs was registered using both implicit (Implicit Association Test, affective priming) and explicit measures (valence ratings). In line with the assumption that EC effects can be based on CS-US pairings that are not directly experienced, the valence of the CSs changed in the direction of the US with which they were covertly paired. This effect was observed both on explicit and on implicit measures. We argue that several aspects of our results are in line with propositional models of EC and fit less well with association formation models.     

Evaluative conditioning without directly experienced pairings of the conditioned and the unconditioned stimuli

Evaluative conditioning (EC) is the valence change of a stimulus (conditioned stimulus, CS) that is due to the previous pairing with another stimulus (unconditioned stimulus, US). We investigated whether EC can occur also when the CS–US pairings are not experienced directly by the participant but are implied by other events that the participant encounters. In two experiments, positive USs were presented in some trials and negative USs in other trials. Afterwards, participants were given information from which it was possible to conclude that CSs were covertly present during these trials. Finally, the valence of these CSs was registered using both implicit (Implicit Association Test, affective priming) and explicit measures (valence ratings). In line with the assumption that EC effects can be based on CS–US pairings that are not directly experienced, the valence of the CSs changed in the direction of the US with which they were covertly paired. This effect was observed both on explicit and on implicit measures. We argue that several aspects of our results are in line with propositional models of EC and fit less well with association formation models.     

The effectiveness of electric shock and foul odor as unconditioned stimuli in classical aversive conditioning

In a partial replication of an earlier study, eighty undergraduate volunteers were assigned to the eight cells of a three between- and two within-group experimental design. One factor was the nature of the UCS—faradic shock or a carefully-timed blast of pyridine vapor; the second factor was the UCS contingency—the UCS being contingent upon the CS or randomly interspersed; the third factor was the nature of the CS—all CSs were compounds of colored, flavored liquids, with the discriminable dimension being either color or taste. The two within-subjects factors were the successive presentation of either the CS+ of the CS? over trials in a standard classical conditioning format. The outcome measures were sip-size, order of preference, and semantic differential ratings. It was found that the foul odor UCS resulted in no aversive conditioning with either color or taste cues. Where shock was the UCS, color, but not taste, became aversive. While lending no direct support to cue-appropriateness concepts, the results reveal the complexity of cue utilization in human aversive conditioning.     

Post-training amphetamine administration enhances memory consolidation in appetitive Pavlovian conditioning: Implications for drug addiction

It has been suggested that some of the addictive potential of psychostimulant drugs of abuse such as amphetamine may result from their ability to enhance memory for drug-related experiences through actions on memory consolidation. This experiment examined whether amphetamine can specifically enhance consolidation of memory for a Pavlovian association between a neutral conditioned stimulus (CS-a light) and a rewarding unconditioned stimulus (US-food), as Pavlovian conditioning of this sort plays a major role in drug addiction. Male Long-Evans rats were given six training sessions consisting of 8 CS presentations followed by delivery of the food into a recessed food cup. After the 1st, 3rd, and 5th session, rats received subcutaneous injections of amphetamine (1.0 or 2.0 mg/kg) or saline vehicle immediately following training. Conditioned responding was assessed using the percentage of time rats spent in the food cup during the CS relative to a pre-CS baseline period. Both amphetamine-treated groups showed significantly more selective conditioned responding than saline controls. In a control experiment, there were no differences among groups given saline, 1.0 or 2.0 mg/kg amphetamine 2 h post-training, suggesting that immediate post-training amphetamine enhanced performance specifically through actions on memory consolidation rather than through non-mnemonic processes. This procedure modeled Pavlovian learning involved in drug addiction, in which the emotional valence of a drug reward is transferred to neutral drug-predictive stimuli such as drug paraphernalia. These data suggest that amphetamine may contribute to its addictive potential through actions specifically on memory consolidation.     

Unblocking in Pavlovian fear conditioning

Six experiments used rats to study blocking and unblocking of fear learning. An excitatory stimulus (A) blocked fear learning to a neutral stimulus (B). Unblocking of B occurred if the AB compound signaled an increase in unconditioned stimulus (US) intensity or number. Assessments of associative change during blocking showed that more was learned about B than A. Such assessments during unblocking revealed that more was learned about B than A following an increase in US intensity but not US number. These US manipulations had no differential effects on single-cue learning. The results show that variations in US intensity or number produce unblocking of fear learning, but for each there is a different profile of associative change and a potentially different mechanism.     

Short-term memory for intonation.

Ss were presented with lists of 16 words, each word spoken in one of four intonations. The final word was a repetition of one of the first 15 words, 40 Ss having to judge whether it was spoken in the same intonation as its earlier occurrence. A control group of 40 Ss did a similar task, ignoring intonation. Retention of intonation was significantly poorer, indicating that intonation is an additional load not normally retained. This argues against acoustic or articulatory encoding in short-term memory and in favor of an abstract-verbal encoding mode. Results are also interpreted as supporting the position that verbal and motor short-term membory obey similar laws.     

Differences in the effect of Pavlovian contingencies upon behavioral momentum using auditory versus visual stimuli.

We examined the role of Pavlovian and operant relations in behavioral momentum by arranging response-contingent alternative reinforcement in one component of a three-component multiple concurrent schedule with rats. This permitted the simultaneous arranging of different response-reinforcer (operant) and stimulus-reinforcer (Pavlovian) contingencies during three baseline conditions. Auditory or visual stimuli were used as discriminative stimuli within the multiple concurrent schedules. Resistance to change of a target response was assessed during a single session of extinction following each baseline condition. The rate of the target response during baseline varied inversely with the rate of response-contingent reinforcement derived from a concurrent source, regardless of whether the discriminative stimuli were auditory or visual. Resistance to change of the target response, however, did depend on the discriminative-stimulus modality. Resistance to change in the presence of visual stimuli was a positive function of the Pavlovian contingencies, whereas resistance to change was unrelated to either the operant or Pavlovian contingencies when the discriminative stimuli were auditory. Stimulus salience may be a factor in determining the differences in resistance to change across sensory modalities.     

A role for CS-US contingency in Pavlovian conditioning

Two experiments evaluated the role of conditioned stimulus-unconditioned stimulus (CS-US) contingency in appetitive Pavlovian conditioning in rats. In both experiments, some groups received a positively contingent CS signaling an increased likelihood of the US relative to the absence of the CS. These groups were compared with control treatments in which the likelihood of the US was the same in the presence and absence of the CS. A trial marker served as a trial context. Experiment 1 found contingency sensitivity. There was a reciprocal relationship between responding to the CS and the trial marker. Experiment 2 showed that this result was not stimulus or response specific. These results are consistent with associative explanations and the idea that rats are sensitive to CS-US contingency.