An immediate-shock freezing deficit with discrete cues: a possible role for unconditioned stimulus processing mechanisms.

Five experiments with C57BL/6 mice (Mus musculus) investigated whether failures in shock processing might contribute to deficits in freezing that occur after an animal receives a shock immediately on exposure to a conditioning context. Experiment 1 found that more contextual freezing resulted from delayed shocks than from immediate shocks across 4 shock intensities. Experiment 2 extended the immediate-shock freezing deficit to discrete stimuli. Experiment 3 found that preexposure to the to-be-conditioned cue did not facilitate immediate cued conditioning. Experiment 4 found that context preexposure enhanced context-evoked fear after an immediate shock. Experiment 5 found that context preexposure also enhanced immediate cued conditioning. These findings are problematic for current theories of the immediate-shock freezing deficit that focus exclusively on processing of the conditioned stimulus, and they suggest that failures in shock processing may contribute to the deficit.     

Effects of multisensory environmental stimulation on contextual conditioning in the developing rat

The effect of increased exposure to multisensory stimulation during development on conditioned freezing to contextual cues in preweanling Sprague-Dawley rats was examined. Rats given increased environmental stimulation exhibited long-term contextual conditioning at a younger age than rats that did not receive such stimulation when there was either low or moderate levels of conditioning (Experiments 1 and 2). These differences in contextual conditioning were not a result of the stimulated rats reacting differently to shock (Experiment 4) or merely freezing more than the nonstimulated rats in all situations (Experiment 3). The role of the glucocorticoid system in the enhanced contextual learning of stimulated preweanling rats and the advantages of the contextual conditioning procedure for studying the effects of environmental stimulation are discussed.     

Ventral and dorsolateral regions of the midbrain periaqueductal gray (PAG) control different stages of defensive behavior: Dorsolateral PAG lesions enhance the defensive freezing produced by massed and immediate shock

Rats that receive nociceptive electric shock in an environment normally show the conditional fear-induced defensive response of freezing when returned to that environment. If several electric shocks are given in a massed manner they will condition less freezing than the same shocks given in a distributed manner. If a single shock is given immediately after placement in the chamber it does not support any conditioning, although the same shock given after a brief delay does. Electrolytic lesions of the dorsolateral periaqueductal gray (PAG), which damaged dorsomedial, dorsolateral, and lateral PAG, enhanced freezing under these conditions. Lesions of the ventral PAG, which caused extensive damage to the central gray below the aqueduct, reduced conditioning under the more optimal parameters (distributed or delayed shock). This was taken to indicate that both of these regions support different modes of defensive behavior and that when activated, the dorsolateral PAG inbits conditional fear-induced defensive behavior. © 1995 Wiley-Liss, Inc.     

Naloxone and shock-elicited freezing in the rat.

The freezing behavior of the rat that occurs following painful electric shock was found to increase when the animal was pretreated with the opiate antagonist naloxone. Freezing was a positive linear function of drug dose and shock intensity (Experiment 2). Naloxone pretreatment enhanced freezing only when the animal was given two or three shocks but did not affect freezing when the animal was given only one shock or not shocked at all (Experiments 3, 4, and 5). Naloxone must be present during shock, nor just during the observation period, in order to increase freezing (Experiment 6). These results suggest that when an animal is shocked, it releases endogenous analgesics (endorphins) that make a subsequent shock less aversive. Naloxone, by blocking the endorphin system, makes the shock more aversive than it would normally be.     

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.     

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.     

Determination of discount functions in rats with an adjusting-amount procedure.

An adjusting-amount procedure was used to measure discounting of reinforcer value by delay. Eight rats chose between a varying amount of immediate water and a fixed amount of water given after a delay. The amount of immediate water was systematically adjusted as a function of the rats' previous choices. This procedure was used to determine the indifference point at which each rat chose the immediate amount and the delayed amount with equal frequency. The amount of immediate water at this indifference point was used to estimate the value of the delayed amount of water. In Experiment 1, the effects of daily changes in the delay to the fixed reinforcer (100 microliters of water delivered after 0, 2, 4, 8, or 16 s) were tested. Under these conditions, the rats reached indifference points within the first 30 trials of each 60-trial session. In Experiment 2, the effects of water deprivation level on discounting of value by delay were assessed. Altering water deprivation level affected the speed of responding but did not affect delay discounting. In Experiment 3, the effects of varying the magnitude of the delayed water (100, 150, and 200 microliters) were tested. There was some tendency for the discounting function to be steeper for larger than for smaller reinforcers, although this difference did not reach statistical significance. In all three experiments, the obtained discount functions were well described by a hyperbolic function. These experiments demonstrate that the adjusting-amount procedure provides a useful tool for measuring the discounting of reinforcer value by delay.     

Effects of Age on the Generalization and Incubation of Memory in the F344 Rat

Freezing (immobility) in the presence of aversive stimuli is a species-specific behavior that is used as an operational measure of fear. Conditioning of this response to discrete sensory stimuli and environmental context cues has been used as a tool to study the neuropsychology of memory dynamics and their development over the lifespan. Three age groups of F344 rats (3, 9, and 27 month) received tone–foot shock pairing (or tone only) in a distinctive chamber on two consecutive days. Separate subgroups of rats from each age group were then tested, at retention intervals of 1, 20, 40, or 60 days, for context-mediated fear in the environment in which they were trained, for generalization of the fear response to a novel chamber, and for fear of the tone. Beginning at day 20, the 27-month-old rats exhibited less freezing behavior than did younger rats when tested in the conditioning context. This age difference was a result of freezing behavior becoming progressively stronger with time in the two younger age groups, a phenomenon that has been referred to as memory incubation. Incubation of the contextual fear response was not detected in the old rats. In a novel context, all age groups exhibited significantly more freezing than did control animals. There was also pronounced incubation of this generalized freezing response, and the extent of incubation declined significantly with age. In the novel context, the freezing response to the tone was robust in all age groups and increased over time, in constant proportion to the degree of freezing elicited by the novel context itself, prior to tone onset. The fact that old animals are known to be relatively selectively impaired in forms of memory that depend on a functional hippocampus suggests a possible explanation for the reduced incubation effects seen in old rats; however, whether the increased expression of fear over time is mediated by a hippocampal-dependent memory consolidation process or whether it reflects a generalized increase in the gain of the circuitry mediating the fear response itself, remains to be determined.     

The effects of early handling on the partial reinforcement extinction effect and the partial punishment effect in male and female rats

Handled (Day 1-22) and non-handled infantile Wistar rats were tested in maturity for the partial reinforcement extinction effect (PREE) and the partial punishment effect (PPE). In Experiments 1 and 2, mature male and female rats were trained to run in an alley for food reward on a 1-trial/day schedule. In the PREE paradigm (Experiment 1), the partially reinforced group (PRF) received reinforcement on a quasi-random 50% schedule, while the continuously reinforced group (CRF) received reinforcement on every trial. In the test stage, both groups were given extinction training. In the PPE paradigm (Experiment 2), the partially punished (PP) group received, together with continuous reinforcement, shocks on a quasirandom 50% schedule, while the continuously reinforced group was reinforced on every trial. In test, all animals were given both reinforcement and shock on every trial. In Experiment 1, PREE—i.e. increased resistance to extinction in the PRF as compared to the CRF group—was more pronounced in the handled animals. More specifically, no PREE was obtained in the non-handled males, and in the non-handled females the PREE was reduced compared to the handled females. The results of Experiment 2 revealed no effect of handling or sex on PPE, that is, increased resistance to punishment in the PP group as compared to the CRF group was evident in all four conditions. In Experiment 3, handled and non-handled male rats were tested for the PREE using a multi-trial procedure in an operant chamber. PREE was obtained in the handled but not in the non-handled animals. The implications of these results for the differential effects of handling on male and female rats and the distinction between the PREE and PPE paradigms are discussed.     

Two tests of the stuck-in-time hypothesis

The authors report 2 experiments that test the stuck-in-time hypothesis, which argues that animals cannot time-date events and thus do not remember when events occurred and do not anticipate future events. In Experiment 1, rats in the experimental condition could earn a large reward by reentering the 1st arm that they visited on a radial maze. They did not learn to reenter this arm early and did no better than did a control group that was not given a large reward for reentering the first arm. In Experiment 2, rats in the experimental group could earn a large reward by delaying entry into a distinctive arm. These rats did not learn to delay entry into the distinctive arm, and they performed no better than did the control-group rats, which did not receive a large reward for delayed entry. These experiments provide further evidence in support of the stuck-in-time hypothesis.     

Effect of delay-interval stimuli on delayed symbolic matching to sample in the pigeon

In Experiment 1, food-deprived pigeons received delayed symbolic matching to sample training in a darkened Skinner box. Trials began with the illumination of the grain feeder lamp (no food sample), or illumination of this lamp, accompanied by the raising of the feeder tray (food sample). After a delay of a few seconds, the two side response keys were illuminated, one with red and one with green light, with positions counterbalanced over trials. Pecking the red (green) comparison produced grain reinforcement if the trial had started with food (no food); pecking red after a no-food sample or green after a food sample was not reinforced. Once matching performance was stable, four stimuli were presented during the delay interval, and their effects on matching accuracy were evaluated. Both illumination of the houselight and the center key with white geometric forms decreased matching accuracy, whereas presentation of a tone and vibration of the test chamber did not. In Experiment 2, pecking the red center key was reinforced with food according to a variable interval schedule. The effects of occasional brief presentations of the four stimuli used in the first experiment on ongoing pecking were assessed. The houselight and form disturbed key pecking, but the tone and vibration did not. Thus, stimuli that interfered with delayed matching also interfered with simple operant behavior. Implications of these results for theories of remembering are discussed.     

Opioid regulation of spinal cord plasticity: evidence the kappa-2 opioid receptor agonist GR89696 inhibits learning within the rat spinal cord

Spinal cord neurons can support a simple form of instrumental learning. In this paradigm, rats completely transected at the second thoracic vertebra learn to minimize shock exposure by maintaining a hindlimb in a flexed position. Prior exposure to uncontrollable shock (shock independent of leg position) disrupts this learning. This learning deficit lasts for at least 24h and depends on the NMDA receptor. Intrathecal application of an opioid antagonist blocks the expression, but not the induction, of the learning deficit. A comparison of selective opioid antagonists implicated the kappa-opioid receptor. The present experiments further explore how opioids affect spinal instrumental learning using selective opioid agonists. Male Sprague-Dawley rats were given an intrathecal injection (30 nmol) of a kappa-1 (U69593), a kappa-2 (GR89696), a mu (DAMGO), or a delta opioid receptor agonist (DPDPE) 10 min prior to instrumental testing. Only the kappa-2 opioid receptor agonist GR89696 inhibited acquisition (Experiment 1). GR89696 inhibited learning in a dose-dependent fashion (Experiment 2), but had no effect on instrumental performance in previously trained subjects (Experiment 3). Pretreatment with an opioid antagonist (naltrexone) blocked the GR89696-induced learning deficit (Experiment 4). Administration of GR89696 did not produce a lasting impairment (Experiment 5) and a moderate dose of GR89696 (6 nmol) reduced the adverse consequences of uncontrollable nociceptive stimulation (Experiment 6). The results suggest that a kappa-2 opioid agonist inhibits neural modifications within the spinal cord.     

Backward Sensory Preconditioning When Reinforcement Is Delayed

In two experiments rats received an initial phase of training in which two neutral stimuli were presented as a serial compound (A-X). In a second phase, Awas established as a signal for a shock reinforcer, the shock being presented immediately after the termination of A (the immediate condition) or after a 5-sec interval (the trace condition). A final test phase showed that not only A but also X was capable of evoking conditioned suppression (a backward sensory preconditioning effect). The degree of suppression evoked by X was not correlated with that evoked by A. In both experiments the A trained with immediate reinforcement was more suppressive than that trained with the trace procedure, but in Experiment 1 the trace and immediate groups did not differ in the response they showed to X, and in Experiment 2 (which allowed a within-subject comparison) the trace procedure resulted in more suppression to X than did immediate conditioning of A. These results disconfirm the suggestion that the backward sensory preconditioning effect depends on the formation of an associative chain: X-A-shock. They are consistent with the proposal that the associatively activated representation of X is able to form a direct association with the reinforcer during A-shock training.     

When people’s judgments of learning (JOLs) are extremely accurate at predicting subsequent recall: the “Displaced-JOL effect”

Judgments of learning (JOL) made after a delay more accurately predict subsequent recall than JOLs made immediately after learning. One explanation is that delayed JOLs involve retrieving information about the target item from secondary memory, whereas immediate JOLs involve retrieval from primary memory. One view of working memory claims that information in primary memory is displaced to secondary memory when attention is shifted to a secondary task. Thus, immediate JOLs might be as accurate as delayed JOLs if an intervening task displaces the target item from primary memory, requiring retrieval from secondary memory, prior to making the JOL. In four experiments, participants saw related word-pairs and made JOLs predicting later recall of the item. In Experiment 1, delayed JOLs were more accurate than JOLs made shortly after learning, regardless of whether a secondary task intervened between learning and JOL. In Experiments 2–4, the secondary task demands increased and JOLs made shortly after learning with an intervening task were just as accurate as delayed JOLs, and both were more accurate than immediate JOLs with no intervening task (Experiment 4). These results are consistent with a retrieval-based account of JOLs, and demonstrate that the “delayed-JOL effect” can be obtained without a long delay.     

Exposure to inescapable shock produces both activity and associative deficits in the rat

Interference with shuttle-box escape learning following exposure to inescapable shock is often difficult to obtain in rats. The first experiment investigated the role of shock intensity during escape training in the apparent fragility of the effect. Experiment 1A demonstrated that the magnitude of the interference effect was systematically related to shock intensity during shuttle-box testing. At .6 mA, a robust effect was obtained, whereas at .8 mA and 1.0, little or no deficit in the escape performance of inescapably shocked rats was observed. Experiment 1B demonstrated that the deficit observed in Experiment 1A depended upon whether or not rats could control shock offset. Experiment 2 suggested that preshock may suppress activity and that higher shock levels may overcome this deficit. Experiment 3 tested this as the sole cause of the escape deficit by requiring an escape response which exceeded the level of activity readily elicited by a 1.0-mA shock in both restrained and preshocked rats. In such a task, preshocked rats performed more poorly than did restrained controls. These results are consistent with the possibility that inescapable shock may, in addition to reducing activity, produce an associative deficit. Experiment 4 more clearly demonstrated that inescapable shock produces deficits in performance which cannot be expleined by activity deficits and which appear to be associative in nature. It was shown that inescapable shock interfered with the acquisition of signaled punishment suppression but not CER suppression. The theoretical implications of these data for explanations of the manner in which prior exposure to inescapable shock interferes with escape learning were discussed.     

Effects of exposure to a to-be-shocked environment upon the rat's freezing response: Evidence for facilitation, latent inhibition, and perceptual learning

Three experiments used the freezing response of rats to examine the effects of pre-exposure to an environment upon (1) its associability with shock and (2) its discriminability from a second environment. Experiments 1 and 2 demonstrated that freezing was proportional to the interval between exposure to the environment at time T1 and the occurrence of shock at T2. This function was shifted by pre-exposure to the to-be-shocked environment, with brief pre-exposures increasing (facilitation) and extended pre-exposures decreasing (latent inhibition) the impact of a given T1-T2 interval on freezing. Experiment 3 provided evidence that the facilitatory and latent inhibitory effects resulting from brief and extended exposures to the to-be-shocked environment were accompanied by an increase in discriminability. The results were taken to have supported the claim that pre-exposure changes associability as well as discriminability (Hall & Honey, 1989) and were discussed in terms of the model for perceptual learning proposed by McLaren, Kaye, and Mackintosh (1990).     

Response-shock delay as a reinforcer in avoidance behavior

After rats received preliminary training to avoid shock on a discrete-trial retractable-bar avoidance procedure, the procedure was changed such that responses retracted the lever but did not affect the rate of shock. Responses only delayed the onset of shock. About half of the animals under these procedures responded consistently on almost 100% of the discrete-trial cycles over days. When short latencies maximized the response-shock delay, animals tended to make short-latency responses. When long latencies maximized the response-shock delay, animals tended to make long-latency responses. When all response latencies produced the same response-shock delay, animals made differing average-latency responses. And, when responses did not delay shock, most of the animals primarily engaged in shock-elicited responding while the other animals engaged in preshock responding.     

An investigation of students' knowledge of the delayed judgements of learning effect

Judgements of learning (JOL) of paired associates can be made immediately after learning or after a delay, while viewing the first word (cue) only or both words (cue–target) in a pair. Delayed cue-only judgements are more related to subsequent memory performance than delayed cue–target, immediate cue-only, or immediate cue–target judgements. In two experiments we tested students' knowledge of this delayed JOL effect and whether their knowledge increases as a function of task experience (Experiment 2). The majority of the participants did not choose the more effective judgement strategy and they did not systematically alter their behaviour as a function of task experience. Instead, a subset of the participants selected judgement strategies on the basis of a learning goal, that is, a strategy that let them restudy both words in a pair. In sum, most students appear to be unaware of the powerful influence of delayed cue-only JOLs on monitoring accuracy.     

Processing of biological motion point-light displays by baboons (Papio papio)

Humans apply complex conceptual judgments to point-light displays (PLDs) representing biological motion (BM), but how animals process this kind of display remains uncertain. Four baboons (Papio papio) were trained to discriminate BM from nonbiological motion PLDs using an operant computerized test system. Transfer tests were given after training with novel BM stimuli representing humans or baboons (Experiment 1), with inverted PLDs (Experiment 2), and with BM stimuli in which body parts had been spatially disorganized (Experiment 3). Very limited transfer was obtained with the novel and inverted displays in Experiments 1 and 2, but transfer was much higher after spatial disorganization in Experiment 3. It is suggested that the baboons did not retrieve and interpret the articulated shape of the human or monkey body from the BM PLD stimuli, but rather focused their attention on the configural properties of subparts of the stimuli. Limits in perceptual grouping and restricted abilities in picture-object equivalence might explain why the baboons did not map BM PLD displays onto what they represent.