Contextual Fear after Signalled versus Unsignalled Shocks: Effect of Extent of Prior Experience with Context and Signal

In the first two experiments, rats were differentially familiarized with a discrete stimulus and/ or a context prior to receiving either shocks signalled by that stimulus or unsignalled shocks in that context. As indexed by freezing, in none of the pre-exposure conditions did the signalled-shock rats consistently acquire less contextual fear than the unsignalled-shock animals. Both pre-exposure to the stimulus and relatively short pre-exposure to the future conditioning context resulted in more contextual fear in the signalled-shock than in the unsignalled-shock subjects. In a third experiment, freezing in the target conditioning context was especially enhanced in rats that had been familiarized with a stimulus, conditioned with the stimulus as a signal for shock, and subsequently further conditioned to the stimulus in a different, non-target context. The level of freezing to the stimulus in a neutral test context was positively related to the level of freezing in the target conditioning context in all experiments. These results were discussed in terms of context-shock, stimulus-shock, and context-stimulus associations.     

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.     

Recent exposure to a dangerous context impairs extinction and reinstates lost fear reactions

Rats were shocked in a context and then exposed to that context in the absence of shock. Shorter intervals between these extinction trials produced more long-term freezing than did longer ones, and shorter intervals between the final extinction trial and test produced more freezing than did longer ones. A short interval between a context extinction trial and test with an extinguished conditioned stimulus (CS) produced more freezing than did a longer one, and a short interval between a nonreinforced context exposure and an extinguished CS reinstated freezing when the CS was tested 24 hr later. The results suggest that recent fear acts to favor subsequent retrieval of the memory formed at conditioning rather than extinction and to render the retrieved memory more salient.     

Footshock intensity and generalization in contextual and auditory-cued fear conditioning in the rat

The relationship between US (footshock) intensity and the two conditioned freezing responses (to acoustic CS and to "context") was investigated in fear conditioning. Administered footshock intensity was 0.00, 0.15, 0.30, 0.60, 0.90, and 1.20 mA to six different groups of 70-day-old male Albino Wistar rats. To measure contextual freezing, the animals were again placed inside the conditioning apparatus without acoustic CS and US presentation. To measure acoustic CS freezing, the animals were placed in a totally different apparatus and only the acoustic CS was presented. The 0.15 mA footshock intensity was not sufficient to condition the animals, in fact no freezing was exhibited as in the non-shocked control group. The 0.30 mA footshock intensity was sufficient only to condition the animals to the acoustic CS, whereas the 0.60 mA was sufficient to condition the animals both to acoustic CS and to context. Footshock intensities (0.90 and 1.20 mA) did not elicit any significant increase in conditioned freezing for either acoustic CS or context but at the highest one the generalization phenomenon appeared (freezing in the different context before presentation of acoustic CS). Acoustic CS freezing to all over-threshold intensities was longer than that to context. In conclusion, freezing responses to acoustic CS and context after increasing footshock intensities follow distinct patterns, and intermediate footshock intensities (0.60 and 0.90 mA) appear to be the most useful for eliciting conditioned freezing responses to acoustic CS and to context without inducing a generalized fear status contamination.     

The hippocampal dentate gyrus is essential for generating contextual memories of fear and drug-induced reward

The hippocampus is believed to play a role in processing information relative to the context in which emotionally salient experiences occur but evidence on the specific contribution of the hippocampal dentate gyrus (DG) to these processes is limited. Here, we have used two classical behavioral paradigms to study the participation of the dorsal DG in context-conditioned reward and context-conditioned fear. Rats received intra-hippocampal vehicle or colchicine injections (4 microg/microl solution; 0.2 microl injections at 10 sites) that damaged the DG but spared other hippocampal subfields. In the first experiment, we used a place conditioning procedure pairing cocaine exposure (20 mg/kg, i.p.) with a specific context and vehicle treatment with another. While rats with sham lesions exhibited preference for the cocaine-paired context following conditioning, rats with lesions of the DG showed no evidence of cocaine-induced place preference. In the second experiment, rats with sham or colchicine lesions received a foot shock in a given context and conditioned freezing was measured upon reexposure to the shock-paired context (2, 24, 48 and 96 h after conditioning). Rats with sham lesions exhibited high levels of conditioned freezing when exposed to the conditioning context but rats with lesions of the DG showed impaired conditioning, behaving as controls that had experienced shock in a different context. These observations indicate that the integrity of the DG is essential for establishing a coherent representation of the context to which emotional experiences, either hedonic or aversive, are bound.     

Super-latent inhibition of conditioned taste preference with a long retention interval

A long delay inserted between conditioning and test phases of a 3-stage Latent Inhibition (LI) procedure produces differential effects on LI depending on the delay context. Thus, enhanced LI has been obtained when the delay is spent in a context that is different from the remaining experimental contexts, but not when it is the same. The present paper examined the effect of delayed testing using a conditioned taste preference procedure. In Experiment 1, three groups received preexposure to either water, or almond, or citrus solutions. Subsequently, the animals were conditioned by pairing the almond and the citrus solutions with sucrose. In a two-bottle preference test conducted 1 day after conditioning, the preexposed flavored solutions were consumed less than the non-preexposed flavors (LI). Experiments 2 and 3 used the same basic procedure, but varied the retention interval duration (1 and 21 days) and the delay context, similar (Experiment 2) and different (Experiment 3) from that of the other stages of the experiments. LI was greater after the long than the short-retention interval when the context was different, thereby demonstrating super-LI. The results were explained by a time-induced context differentiation process.     

Contextual potentiation of acquired behavior after devaluing direct context-US associations

In two experiments, water-deprived rats were exposed to tone-footshock pairings in a particular conditioning context. In Experiment 1, the training parameters were selected on the basis of parametric pilot data so as not to produce direct associations between the conditioning context and footshock. Despite independent evidence of no appreciable direct association between the conditioning context and footshock, animals tested in the conditioning context exhibited more lick suppression to the tone than other animals tested with the tone outside of the conditioning context. Thus, the conditioning context potentiated suppression to the tone in the absence of appreciable fear of the conditioning context. In Experiment 2, training parameters were used that permitted the formation of direct associations between the conditioning context and footshock; however, for half the animals, these associations to the context were then extinguished. With the tone absent, a comparison of extinguished animals tested either in the conditioning context or outside the conditioning context detected no differences in suppression, demonstrating the effectiveness of the extinction manipulation. However, other animals also subjected to extinction of direct context-footshock associations displayed greater suppression to the tone within the conditioning context than comparable animals tested outside the context. Collectively the data indicate that the superior retention-test performance seen within the training context can arise both from the commonly assumed direct associations between the training context and the unconditioned stimulus and from the potentiation by the training context of the associations between the nominal conditioned stimulus and unconditioned stimulus.     

Exteroceptive context in tasteaversion conditioning and extinction: odour, cage, and bottle stimuli

Five experiments investigated the extent to which the exteroceptive context, present on a saccharin aversion conditioning trial with rats, controlled the resulting aversion on one-bottle extinction tests and subsequent preference tests. The presence or absence of the specific odour which had been present on the conditioning trial was found not to influence saccharin intake on extinction tests, whereas the presence of the particular compartment in which, and the bottle from which, the saccharin had been consumed greatly suppressed saccharin intake as compared to the absence of these elements. Preference tests, performed in the respective conditioning contexts, showed extinction to be specific to the compartment + bottle context: groups that had extinguished their saccharin aversion in a context different from the conditioning context, retained their aversion in the conditioning context. No such specificity was found for the odour context. However, in the absence of the taste stimulus during the extinction phase, the odour that had been present on the conditioning trial did control the amount of water consumed, whereas the compartment+bottle context did not. Moreover, on preference tests, groups that had consumed water during extinction in the presence of the odour context, evidenced a lesser saccharin aversion than groups not exposed to the odour. The results are interpreted as demonstrating that rats learn about taste, odour, cage and bottle stimuli on a taste-aversion conditioning trial, and that taste and bottle stimuli seem to be the most salient.     

Genetic background differences and nonassociative effects in mouse trace fear conditioning

Fear conditioning, including variants such as delay and trace conditioning that depend on different neural systems, is widely used to behaviorally characterize genetically altered mice. We present data from three strains of mice, C57/BL6 (C57), 129/SvlmJ (129), and a hybrid strain of the two (F(1) hybrids), trained on various versions of a trace fear-conditioning protocol. The initial version was taken from the literature but included unpaired control groups to assess nonassociative effects on test performance. We observed high levels of nonassociative freezing in both contextual and cued test conditions. In particular, nonassociative freezing in unpaired control groups was equivalent to freezing shown by paired groups in the tests for trace conditioning. A number of pilot studies resulted in a new protocol that yielded strong context conditioning and low levels of nonassociative freezing in all mouse strains. During the trace-CS test in this protocol, freezing in unpaired controls remained low in all strains, and both the C57s and F(1) hybrids showed reliable associative trace fear conditioning. Trace conditioning, however, was not obtained in the 129 mice. Our findings indicate that caution is warranted in interpreting mouse fear-conditioning studies that lack control conditions to address nonassociative effects. They also reveal a final set of parameters that are important for minimizing such nonassociative effects and demonstrate strain differences across performance in mouse contextual and trace fear conditioning.     

Naloxone and Pavlovian fear conditioning

Previous research has shown that pretreating rats with the opiate antagonist naloxone increases the freezing that follows painful electric shock. Three experiments, using freezing behavior as a dependent variable, were carried out to determine whether the drug might cause this effect by enhancing fear conditioning. Two of the studies employed a differential context fear-conditioning paradigm. Naloxone did not affect freezing behavior during the preshock adaptation period. In Experiment 1, naloxone was found to increase resistance to extinction in the S+ context. In Experiment 2, naloxone was found to increase freezing in the S+ context. This effect was dependent upon administering naloxone during training but not dependent on administering it during testing. The third study employed a generalization paradigm. It was found that naloxone's effect on postshock freezing was dependent on the place of testing; as the contextual cues of the test chamber were changed from those of the conditioning chamber, the effect of naloxone on freezing was reduced. The results of these experiments lend strong support to the hypothesis that naloxone increases freezing by enhancing the conditioning of fear to contextual stimuli associated with shock.     

A short intertrial interval facilitates acquisition of context-conditioned fear and a short retention interval facilitates its expression

Rats were shocked in a context on two occasions and then tested for fear reactions as indexed by freezing. Rats spent the interval between conditioning trials and between conditioning and test in their home cages. A short interval between context-conditioning trials or between trials involving a discrete conditioned stimulus (CS) produced better learning than longer intervals. A short retention interval between conditioning and test produced better performance than longer intervals. The effects of the intertrial interval on learning are the opposite of those reported previously and are opposite to those predicted by contemporary learning theories. The effects of the training to test interval on performance are predicted by Wagner's sometimes opponent process (SOP) theory (Wagner, 1981).     

Selective association learning in the rat: Generality of response system

Three experiments with rats examined the possibility that the cue-consequence specificity effect is not mediated by the conditioning of selective associations, but instead reflects the selective behavioral expression of taste-illness and exteroceptive-shock conditioning. Experiment 1 showed that the selective aversion performance could be obtained despite the use of locomotor withdrawal from the CS as the index of conditioning. Experiment 2 compared the response profiles of animals conditioned with footshock or illness to presentation of a saccharin or noise CS. During the test with the noise CS, lithium-conditioned subjects did not differ from control rats on any of several behavioral categories, but shock-conditioned rats showed high levels of freezing in response to the noise cue. During the saccharin test, lithium-treated rats engaged in behaviors such as chin wiping, head shaking, and gaping; these behaviors were rarely or never seen in shock-conditioned rats or controls, whose behavioral profiles during the saccharin test were almost identical. Experiment 3, using a blocking design, found that a noise-lithium pairing did not attenuate subsequent conditioning of a saline-lithium association, nor did a saccharin-shock pairing interfere with conditioning of a noise-shock association. These results confirm that the cue-consequence specificity effect is mediated by the selective associability of taste with illness and of exteroceptive cues with footshock.     

Context extinction following conditioning with delayed reward enhances subsequent instrumental responding

In Experiment 1, delayed reward generated low response rates relative to immediate reward delivered with the same frequency. Lister rats exposed to delayed reward subsequently responded at a higher rate in extinction if they received nonreinforced exposure to the conditioning context after instrumental training and prior to test, compared with animals that received home cage exposure. In Experiment 2, a signaled delay of reinforcement resulted in higher rates than an unsignaled delay. Nonreinforced exposure to the conditioning context elevated response rate for subjects in the unsignaled condition relative to a home cage group, but had no effect on response rates for subjects that had received the signaled delay. In Experiment 3, following an unsignaled reinforcement delay, groups receiving either no event or signaled food in the context responded faster in extinction than groups receiving no context exposure or unsignaled food.     

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.     

Conditioned taste aversion is enhanced when the unconditioned stimulus is presented in a different context

Using a conditioned taste aversion procedure with rats as the subjects, two experiments examined the effect of presenting a conditioned stimulus (CS saccharin solution) in one context followed by an unconditioned stimulus (US LiCl) in a different context. Experiment 1 showed that animals which received the above-mentioned procedure (Group D) showed a more marked conditioned aversion to the CS than animals which were given both the CS and the US in the same context (Group S). Experiment 2 found that in both Group D and Group S, aversion to the CS increased when the subjects were exposed to the conditioned context after the conditioning. These findings supported the argument that the strength of the CS-US association acquired during conditioning is compared with that of the context-US to determine the magnitude of aversion revealed to the CS.     

Potentiation by a taste of toxicosis-based context conditioning: Effects of varying the test fluid

Rats that drank water in a distinctive environment and were then injected with lithium chloride (water-lithium condition) were compared with those given an added taste on those conditioning sessions (sucrose-lithium condition). In three experiments this taste potentiated a conditioned aversion to the context, as measured by suppression of intake of another solution: either a novel sour taste (Experiments 1 and 2) or a familiar saline solution (Experiment 3). In contrast, this potentiation effect was not detected when subjects were tested with water, whether a high or low dose of lithium was used (Experiment 2). Instead, in Experiments 1 and 2 water-lithium subjects drank less water than did the sucrose-lithium subjects on such tests i.e. an apparent overshadowing effect, which was the opposite outcome to that found previously using almost identical procedures. Intake on recovery sessions in another context suggested that, when water is used as the test fluid, potentiation can be masked by two factors: a context-dependent aversion to water in water-lithium subjects, and a conditioned inhibition effect of water in sucrose-lithium subjects. These may account for previous failures to detect potentiation of context conditioning.     

Palatability shifts in taste and flavour preference conditioning

Changes in palatability of tastes and flavours as a result of flavour preference conditioning were examined. In Experiment 1, when tastes were paired with glucose in a reverse-order differential conditioning paradigm, rats acquired conditioned preferences for CS + and displayed more hedonic responses to CS + than to CS - in a postconditioning taste reactivity test. In Experiment 2, rats that received oral infusions of flavours as CSs during a reverse-order conditioning procedure expressed both palatability shifts and conditioned preferences for CS + . Rats that received a forward conditioning procedure acquired a preference for CS + , but the palatability of CS + was unchanged. In Experiment 3, hungry rats drank mixtures of a flavour CS and a calorific or sweet tasting reinforcer in a long-exposure conditioning paradigm. When tested hungry, rats preferred CS + whether they had acquired flavour-calorie or flavour-taste associations. However, CS + became more palatable only for rats that acquired flavour-calorie associations. These results suggest that acquisition of flavour preferences, as measured by 2-bottle tests, may not always be accompanied by enhanced palatability.     

Temporally graded,context-specific retrograde amnesia and its alleviation by context preexposure: effects of postconditioning exposures to morphine in the rat

Five experiments studied retrograde impairments in Pavlovian fear conditioning following prolonged exposure to the opioid receptor agonist morphine. Injections of morphine commencing 1-7 days but not 14 days after conditioning produced amnesia for that conditioning episode. This amnesia was (a) selective such that morphine impaired freezing to the conditioning context but not to the auditory conditioned stimulus, (b) independent of the interval between the last injection of morphine and test, and (c) accompanied by a failure of contextual discrimination. Context preexposure protected context conditioning and discrimination from the amnestic effects of morphine. These results show that retrograde deficits in contextual fear conditioning are mediated by failures to consolidate a contextual representation.     

Post-training ethanol disrupts trace conditioned fear in rats: effects of timing of ethanol, dose and trace interval duration

Ethanol has complex effects on memory performance, although hippocampus-dependent memory may be especially vulnerable to disruption by acute ethanol intoxication occurring during or shortly after a training episode. In the present experiments, the effects of post-training ethanol on delay and trace fear conditioning were examined in adolescent rats. In Experiment 1, 30-day-old Sprague-Dawley rats were given delay or trace conditioning trials in which a 10s flashing light CS was paired with a 0.5 mA shock US. For trace groups, the trace interval was 10 s. On days 31-33, animals were administered ethanol once daily (0.0 or 2.5 g/kg via intragastric intubation), and on day 34 animals were tested for CS-elicited freezing. Results showed that post-training ethanol affected the expression of trace, but had no effect on delay conditioned fear. Experiment 2 revealed that this effect was dose-dependent; doses lower than 2.5 g/kg were without effect. Experiment 3 evaluated whether proximity of ethanol to the time of training or testing was critical. Results show that ethanol administration beginning 24h after training was more detrimental to trace conditioned freezing than administration that was delayed by 48 h. Finally, in Experiment 4 animals were trained with one of three different trace intervals: 1, 3 or 10s. Results indicate that post-training administration of 2.5 g/kg ethanol disrupted trace conditioned fear in subjects trained with a 10s, but not with a 1 or 3s, trace interval. Collectively the results suggest that ethanol administration impairs post-acquisition memory processing of hippocampus-dependent trace fear conditioning.     

Effects of environmental enrichment on rate of contextual processing and discriminative ability in adult rats

The effect of environmental enrichment on conditioned freezing to contextual cues in adult Sprague-Dawley rats was examined. The freezing of both enriched-and standard-reared rats increased with the time spent in the chamber prior to shock. Both groups of rats showed equally low levels of contextual conditioning following a preshock period of 4 s and equally high levels following a 120-s preshock period. However, following a preshock period of 16 s enriched rats displayed more contextual conditioning than standard rats. That is, enriched rats appeared to process contextual information faster than their standard-reared counterparts. Enriched- reared rats also showed a greater ability to discriminate between the conditioning context and a similar but distinctive context. Hence, in addition to forming a representation of the context in memory more rapidly than standard-reared rats, enriched-reared rats also appear to form a more complex representation.