Temporally massed CS presentations generate more fear extinction than spaced presentations

Rodent fear conditioning models both excitatory learning and the pathogenesis of human anxiety, whereas extinction of conditional fear is a paradigm of inhibitory learning and the explicit model for behavior therapy. Many studies support a general learning rule for acquisition: Temporally spaced training is more effective than massed training. The authors asked whether this rule applies to extinction of conditional fear in mice. The authors find that both short- and long-term fear extinction are greater with temporally massed presentations of the conditional stimulus (CS). The data also indicate that once CS presentations are sufficiently massed to initiate, or "induce," extinction learning, further CS presentations are more effective when spaced.     

Trial spacing is a determinant of cue interaction

Four conditioned lick suppression experiments with rats examined the effect of trial spacing on cue interaction. Experiments 1 and 2 found overshadowing to be eliminated with massed compound stimulus-outcome pairings and the usual trial spacing effect to be reversed with compound acquisition trials. Experiment 3 found that whether acquisition compound-outcome pairings were massed or spaced determined the effect of posttraining extinction treatment. Extinction of the overshadowing cue reduced responding following massed training and increased responding following spaced training. Extinction of the context decreased responding following massed training. Experiment 4 found the conditioning and devaluation results to be associative and stimulus specific. These results are in accord with the extended comparator hypothesis (J. C. Denniston, H. I. Savastano, & R. R. Miller, 2001).     

Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice

Extinction of conditioned fear in animals is the explicit model of behavior therapy for human anxiety disorders, including panic disorder, obsessive-compulsive disorder, and post-traumatic stress disorder. Based on previous data indicating that fear extinction in rats is blocked by quinpirole, an agonist of dopamine D2 receptors, we hypothesized that blockade of D2 receptors might facilitate extinction in mice, while agonists should block extinction, as they do in rats. One day after fear conditioning mice with three pairings of a white noise conditional stimulus (CS) with moderate footshock, we injected the D2 antagonist, sulpiride, the D2 agonist, quinpirole, or vehicle, just before repeated CS presentations to generate extinction. We assayed fear by measuring behavioral freezing during extinction presentations and then drug-free during CS presentations 1 d later. We found that sulpiride injections before extinction training facilitated extinction memory 24 h later, while quinpirole partially blocked extinction memory compared with vehicle-injected controls. Notably, sulpiride treatment yielded significant extinction after spaced CS presentations, which yield no extinction at all in vehicle-treated mice. These findings suggest that dopamine D2-mediated signaling contributes physiological inhibition of extinction, and that D2 antagonists may be useful adjuncts to behavior therapy of human anxiety disorders.     

The exemplar interleaving effect in inductive learning: Moderation by the difficulty of category discriminations

Recent research demonstrates a spacing effect in inductive learning. Spacing different individual exemplars apart in time, rather than massing them together, aids in the learning of categories. Experiment 1 examined whether it is interleaving or temporal spacing that is critical to the spacing effect in the situation wherethe memory load is high, and the results favored interleaving. Experiment 2 examined the effect of the difficulty of the category discrimination on presentation style (massed vs. spaced) in inductive learning, and the results demonstrated that spacing (i.e., interleaving of exemplars from different categories) is advantageous for low-discriminabilty categories, whereas massing is more effective for high-discriminability categories. In contrast to these performance measures, massing was judged by participants to be more effective than spacing in both discriminability conditions, even when performance for low-discriminability categories showed the opposite.     

Amygdala and hippocampal activity during acquisition and extinction of human fear conditioning

Previous functional magnetic resonance imaging (fMRI) studies have characterized brain systems involved in conditional response acquisition during Pavlovian fear conditioning. However, the functional neuroanatomy underlying the extinction of human conditional fear remains largely undetermined. The present study used fMRI to examine brain activity during acquisition and extinction of fear conditioning. During the acquisition phase, participants were either exposed to light (CS) presentations that signaled a brief electrical stimulation (paired group) or received light presentations that did not serve as a warning signal (control group). During the extinction phase, half of the paired group subjects continued to receive the same treatment, whereas the remainder received light alone. Control subjects also received light alone during the extinction phase. Changes in metabolic activity within the amygdala and hippocampus support the involvement of these regions in each of the procedural phases of fear conditioning. Hippocampal activity developed during acquisition of the fear response. Amygdala activity increased whenever experimental contingencies were altered, suggesting that this region is involved in processing changes in environmental relationships. The present data show learning-related amygdala and hippocampal activity during human Pavlovian fear conditioning and suggest that the amygdala is particularly important for forming new associations as relationships between stimuli change.     

Stress-enhanced fear learning in rats is resistant to the effects of immediate massed extinction

Enhanced fear learning occurs subsequent to traumatic or stressful events and is a persistent challenge to the treatment of post-traumatic stress disorder (PTSD). Facilitation of learning produced by prior stress can elicit an exaggerated fear response to a minimally aversive event or stimulus. Stress-enhanced fear learning (SEFL) is a rat model of PTSD; rats previously exposed to the SEFL 15 electrical shocks procedure exhibit several behavioral responses similar to those seen in patients with PTSD. However, past reports found that SEFL is not mitigated by extinction (a model of exposure therapy) when the spaced extinction began 24?h after stress. Recent studies found that extinction from 10?min to 1?h subsequent to fear conditioning "erased" learning, whereas later extinction, occurring from 24 to 72?h after conditioning did not. Other studies indicate that massed extinction is more effective than spaced procedures. Therefore, we examined the time-dependent nature of extinction on the stress-induced enhancement of fear learning using a massed trial's procedure. Experimental rats received 15 foot shocks and were given either no extinction or massed extinction 10?min or 72?h later. Our present data indicate that SEFL, following traumatic stress, is resistant to immediate massed extinction. Experimental rats showed exaggerated new fear learning regardless of when extinction training occurred. Thus, post-traumatic reactivity such as SEFL does not seem responsive to extinction treatments.     

Electrolytic lesions of the dorsal hippocampus disrupt renewal of conditional fear after extinction

There is a growing body of evidence that the hippocampus is critical for context-dependent memory retrieval. In the present study, we used Pavlovian fear conditioning in rats to examine the role of the dorsal hippocampus (DH) in the context-specific expression of fear memory after extinction (i.e., renewal). Pre-training electrolytic lesions of the DH blunted the expression of conditional freezing to an auditory conditional stimulus (CS), but did not affect the acquisition of extinction to that CS. In contrast, DH lesions impaired the context-specific expression of extinction, eliminating the renewal of fear normally observed to a CS presented outside of the extinction context. Post-extinction DH lesions also eliminated the context dependence of fear extinction. These results are consistent with those using pharmacological inactivation of the DH and suggest that the DH is required for using contextual stimuli to regulate the expression of fear to a Pavlovian CS after extinction.     

The incubation theory of fear/anxiety: experimental investigation in a human laboratory model of Pavlovian conditioning

The aim of this work was to test Eysenck's incubation theory of fear/anxiety in human Pavlovian B conditioning of heart rate (HR) responses. The conditioned stimuli (CSs) were phobia-relevant slides (snakes and spiders) and the unconditioned stimuli (UCSs) were aversive noises. The subjects were presented with two levels of noise intensity during acquisition and three levels of nonreinforced CS presentation (CS-only) in a delay differential (CS+/CS-) conditioning paradigm (2 x 3 x 2). Consistent with the incubation theory, conditioned HR acceleratory responses were sustained (resistance to extinction) for high-noise intensity and short-presentations of CS-only subjects. During the extinction phase, HR acceleratory responses quickly extinguished in low-noise intensity groups after the first presentations of CS-only. These findings were interpreted as support for the incubation theory of phobic fear.     

Conducting extinction in multiple contexts does not necessarily attenuate the renewal of shock expectancy in a fear-conditioning procedure with humans

The renewal of Pavlovian-conditioned responses may provide a model for the relapse of fear following extinction-based treatments for anxiety disorders. Renewal can be observed if conditional stimulus (CS) and unconditional stimulus (US) pairings are given in one context, extinction trials of CS presentations in a second context, prior to test trials of CS presentations in the original acquisition context (ABA renewal). We examined ABA renewal in humans by using a fear-conditioning procedure with an unpleasant shock US. A renewal of rated shock expectancy was demonstrated with this procedure. Conducting extinction treatment in multiple contexts was expected to attenuate the renewal effect. However, the renewal of shock expectancy persisted when extinction treatment was given across three or five different contexts. With the current renewal design, learning task, and measure of conditioned behaviour, extinction treatment does not appear to readily generalise to the test context. The use of multiple extinction treatments in a clinical setting may not necessarily reduce the likelihood of relapse via a renewal effect.     

Spacing one's study: evidence for a metacognitive control strategy

This article investigated individual control of spacing strategies during study. Three predictions were outlined: The spacing hypothesis suggests that people choose to space their study to improve long-term learning via the spacing effect. The massing hypothesis suggests that people choose to mass their study because of illusions of confidence during study. The metacognitive hypothesis suggests that people control their spacing schedules as a function of their metacognitive judgments of specific to-be-learned items. To test these hypotheses, the authors asked participants to study and make judgments of learning for cue-target pairs. Then, participants were given three choices; they could study the pair again immediately (massed), study the pair again after the entire list had been presented (spaced), or choose not to restudy (done). Results supported a metacognitively controlled spacing strategy-people spaced items that were judged to be relatively easy but massed items that were judged as relatively difficult.     

Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction

After extinction of fear to a Pavlovian conditional stimulus (CS), contextual stimuli come to regulate the expression of fear to that CS. There is growing evidence that the context dependence of memory retrieval after extinction involves the hippocampus. In the present experiment, we examine whether hippocampal involvement in memory retrieval after extinction is related to the history of CS presentations in the context used for retrieval testing. We used infusions of muscimol to inactivate the dorsal hippocampus (DH) during postextinction retrieval tests that were conducted in contexts that differed in their history of CS presentations in that context. We found that DH inactivation affected the context-dependent retrieval of extinction (i.e., renewal) when testing occurred in a context that had no history of CS exposure, but not in a context that reliably predicted the CS. These results are discussed in terms of theories regarding the role of the hippocampus in contextual memory retrieval.     

Spreading the words: A spacing effect in vocabulary learning

The spacing effect refers to the frequently observed finding that distributing learning across time leads to better retention than massing it into one single study session. In the present study, we examined whether the spacing effect generalises to primary school vocabulary learning. To this aim, children from Grade 3 were taught the meaning of 15 new words using a massed procedure and 15 other new words using a spaced procedure. The 15 words in the massed condition were divided into three sets of five words, and each set was taught three times in one of three learning sessions. In the spaced condition, learning was distributed across the three sessions: All 15 words were practised once in each of the three learning sessions. At the retention tests after 1 week and after 5 weeks we observed that the meaning of spaced words was remembered better than the meaning of massed words.     

Learning concepts and categories: is spacing the "enemy of induction"?

Inductive learning -- that is, learning a new concept or category by observing exemplars -- happens constantly, for example, when a baby learns a new word or a doctor classifies x-rays. What influence does the spacing of exemplars have on induction? Compared with massing, spacing enhances long-term recall, but we expected spacing to hamper induction by making the commonalities that define a concept or category less apparent. We asked participants to study multiple paintings by different artists, with a given artist's paintings presented consecutively (massed) or interleaved with other artists' paintings (spaced). We then tested induction by asking participants to indicate which studied artist (Experiments 1a and 1b) or whether any studied artist (Experiment 2) painted each of a series of new paintings. Surprisingly, induction profited from spacing, even though massing apparently created a sense of fluent learning: Participants rated massing as more effective than spacing, even after their own test performance had demonstrated the opposite.     

Contrasting reduced overshadowing and blocking

Preexposure of a cue without an outcome (X-) prior to compound pairings with the outcome (XZ-->O) can reduce overshadowing of a target cue (Z). Moreover, pairing a cue with an outcome (X-->O) before compound training can enhance its ability to compete with another cue (i.e., blocking). Four experiments were conducted in a conditioned bar-press suppression preparation with rats to determine whether spacing of the X- or X-->O trials would differentially affect reduced overshadowing and blocking. Experiment 1a showed that reduced overshadowing was larger with massed trials than with spaced trials. Experiment 1b found that blocking was larger with spaced trials than with massed trials. Experiments 2a and 2b indicated that these effects of trial spacing were both mediated by the associative status of the context at test. The results are interpreted in the framework of contemporary learning theories.     

Priming and trial spacing in extinction: Effects on extinction performance,spontaneous recovery,and reinstatement in appetitive conditioning

Previous research in this laboratory suggests that priming of the conditional stimulus (CS) in short-term memory may play a role in the trial-spacing effects in appetitive conditioning. For example, a nonreinforced presentation of a CS 60 s before a reinforced trial with the same CS produced slower acquisition than a CS presentation that occurred 240 s before the reinforced trial. The results were consistent with the self-generated priming mechanism proposed by Wagner (e.g., Wagner 1978, 1981). The present experiments extended the earlier work by examining the effects of trial spacing in extinction rather than acquisition. After conditioning with a mixture of intertrial intervals (ITIs), rats received extinction with ITIs of 60 or 240 s, longer or shorter values, or different ways of “chunking” extinction trials in time. Although trial spacing produced effects on extinction performance that were consistent with our previous research on acquisition, there were few long-term differences in spontaneous recovery or in reinstatement. Short ITIs in extinction appear to affect extinction performance more than they affect extinction learning. Mechanisms of trial spacing in conditioning and extinction are discussed.     

Distributed practice in verbal recall tasks: A review and quantitative synthesis

The authors performed a meta-analysis of the distributed practice effect to illuminate the effects of temporal variables that have been neglected in previous reviews. This review found 839 assessments of distributed practice in 317 experiments located in 184 articles. Effects of spacing (consecutive massed presentations vs. spaced learning episodes) and lag (less spaced vs. more spaced learning episodes) were examined, as were expanding interstudy interval (ISI) effects. Analyses suggest that ISI and retention interval operate jointly to affect final-test retention; specifically, the ISI producing maximal retention increased as retention interval increased. Areas needing future research and theoretical implications are discussed.     

Examination of a backchaining/counterconditioning process during the extinction of conditioned fear

Two experiments using rat subjects are reported which attempt to delineate the theoretical mechanisms involved in exposure/extinction procedures that are used to eliminate conditioned fear. In Experiment 1, a within-subjects design was employed to study the temporal course of the extinction process by examining the relationship among three separate measures of classically conditioned fear--suppression of an ongoing, operant behavior during the nonreinforced fear-eliciting CS presentation, the time to the first response during this CS presentation, and the time to recover responding following termination of the CS. The results indicated a temporal relationship among these measures, both within and across nonreinforced CS trials, which were considered to reflect a backchaining of a fear-antagonistic response during extinction, and provided an empirical demonstration of an extinction process consistent with Denny's (Behaviour Therapy and Experimental Psychiatry, 7, 315-321, 1976) elicitation/backchaining explanation of extinction. Experiment 2 attempted to manipulate the course of extinction and the temporal relationship among these three fear measures through the paired presentations of the fear CS with a palatable substance (maltose). This procedure produced greater extinction apparently by facilitating the backchaining process. These results are discussed with implications for exposure-based therapies.     

Priming and trial spacing in extinction: effects on extinction performance, spontaneous recovery, and reinstatement in appetitive conditioning

Previous research in this laboratory suggests that priming of the conditional stimulus (CS) in short-term memory may play a role in the trial-spacing effects in appetitive conditioning. For example, a nonreinforced presentation of a CS 60 s before a reinforced trial with the same CS produced slower acquisition than a CS presentation that occurred 240 s before the reinforced trial. The results were consistent with the self-generated priming mechanism proposed by Wagner (e.g., Wagner 1978, 1981). The present experiments extended the earlier work by examining the effects of trial spacing in extinction rather than acquisition. After conditioning with a mixture of intertrial intervals (ITIs), rats received extinction with ITIs of 60 or 240 s, longer or shorter values, or different ways of “chunking” extinction trials in time. Although trial spacing produced effects on extinction performance that were consistent with our previous research on acquisition, there were few long-term differences in spontaneous recovery or in reinstatement. Short ITIs in extinction appear to affect extinction performance more than they affect extinction learning. Mechanisms of trial spacing in conditioning and extinction are discussed.     

Parallel effects of aging and time pressure on memory for source: evidence from the spacing effect

Two experiments address the degree to which item memory-the ability to remember that a word has been presented-is dissociable from source memory, or the ability to remember the context of that word's presentation. Spacing (as opposed to massing) an item's two presentations leads young adults to endorse that item more often when they are instructed to recognize it and to reject it more often when they are instructed to exclude it. Old adults also enjoy beneficial effects of spacing when the item is to be recognized, but suffer detrimental effects of the spacing manipulation when the item is to be rejected: They falsely endorse the spaced to-be-rejected items more than the massed ones. This dissociation also obtains with young subjects under conditions of increased time pressure: Under normal decision conditions, the ability to endorse to-be-recognized items and to reject to-be-rejected items increases with spacing; under speeded conditions, the ability to reject the latter items decreases with spacing. The results support the notion that source memory is selectively impaired in the elderly and that it is difficult to access mnemonic information about source under time pressure.     

Reward schedule effects in extinction: Intertrial interval, memory, and memory retrieval

Rats were trained in a runway such that partial reward occurred on Trial 1 of the day and consistent reward on subsequent massed trials (Group PRT1), or consistent reward occurred on Trial 1 of the day and partial reward on subsequent massed trials (Group PRTM). Under spaced (24-hr) extinction, Group PRT1 was more resistant to extinction than Group PRTM and under massed (1-min) extinction, Group PRTM was more resistant to extinction than Group PRT1. These findings suggest that (a) distinctive stimuli are associated with Trial 1 of the day and with subsequent massed trials, (b) these distinctive stimuli function as retrieval cues for memories, memory retrieval being independent of intertrial interval, and (c) behavior in extinction is controlled by a stimulus compound consisting of the memory of nonreward plus stimuli which accompany the memory of nonreward on rewarded acquisition trials.