Effects of emotional arousal on multiple memory systems: evidence from declarative and procedural learning

Extensive evidence documents emotional modulation of hippocampus-dependent declarative memory in humans. However, little is known about the emotional modulation of striatum-dependent procedural memory. To address how emotional arousal influences declarative and procedural memory, the current study utilized (1) a picture recognition and (2) a weather prediction (WP) task (a probabilistic classification learning task), which have been shown to rely on hippocampal- and striatum-based memory systems, respectively. Observers viewed arousing or neutral pictures after (Experiment 1) or during (Experiment 2) WP training trials. A 1-wk delayed picture recognition memory test revealed enhanced declarative memory for arousing compared with neutral pictures. Arousal during encoding impaired initial WP acquisition but did not influence retention when tested after a 1-wk delay. Data from a subsequent 3-mo delayed test, however, suggested that arousal during acquisition may enhance remote WP retention. These results suggest a potential dissociation between how readily emotional arousal influences hippocampus-dependent and striatum-dependent memory systems in humans.     

Cognitive Procedural Learning in Amnesia

This group study examined the role of residual declarative memory and task-specific cognitive abilities for cognitive procedural learning in amnesia. 20 amnesic patients and 40 control subjects were studied, using four new cognitive tasks, as well as the Tower of Hanoi and a Mirror Reading task. On the cognitive tasks, but not on Mirror Reading, the learning of amnesic patients was significantly impaired relative to controls. Between- and within-group differences in learning were found to be statistically related to cognitive abilities that are involved in the processing of the procedural tasks. In amnesic patients, significant effects of residual declarative memory on learning scores were not observed, but there was indirect evidence for a role of memory in two tasks. The analysis of the correlative relationship between absolute procedural task performances and cognitive abilities indicated a prolonged dependence on nonspecific intellectual abilities in amnesic patients, suggesting a retarded transition to more advanced stages of skill acquisition.     

Emotional enhancement effect of memory: removing the influence of cognitive factors

According to the modulation hypothesis, arousal is the crucial factor in the emotional enhancement of memory (EEM). However, the multifactor theory of the EEM recently proposed that cognitive characteristics of emotional stimuli, e.g., relatedness and distinctiveness, also play an important role. The current study aimed to investigate the individual contribution of arousal to the neural correlates of the EEM by controlling for these additional cognitive factors. We observed the characteristic neuronal correlates of the EEM, in particular enhanced activity in the amygdala and hippocampus, which provides evidence for an arousal-driven EEM in the amygdala as proposed by the modulation hypothesis.     

Forgetting and learning potentiation: dual consequences of between-session delays in cognitive skill learning

In the cognitive skill literature, between-session delays have been treated either as having a negligible effect on performance or as causing forgetting. In contrast, in the procedural skill literature, overnight between-session delays can result in performance gains. In 5 multi-session data sets, the author demonstrates that neither of these 2 models holds for the case of cognitive skill learning. Instead, the delay between sessions appeared to yield both forgetting and enhanced potential for new learning. Two candidate classes of explanation are considered, and implications for the empirical law of learning are discussed.     

The assessment of cognitive procedural learning in amnesia: why the tower of Hanoi has fallen down

The Tower of Hanoi has been widely accepted as an evaluation of cognitive procedural learning in amnesia but inconsistent findings have raised questions about the nature of the learning process involved in this task. This article presents the performance of a hippocampal amnesic, MS, who, showing poor learning across daily sessions of a formal evaluation, subsequently solved the puzzle through spontaneous use of a declarative-level strategy (the odd-even rule), suggesting that his primary approach to the task was the deployment of declarative solution-searching strategies. The presented data suggest normal learning within daily sessions, but subnormal learning across daily sessions due to the forgetting of acquired declarative information. It is suggested that tasks that are potentially solvable by an algorithm or rule, as is the Tower of Hanoi, be regarded as inappropriate for use in cognitive procedural assessments.     

Cognitive procedural learning in early Alzheimer's disease: impaired processes and compensatory mechanisms

Introduction. The aim of this study was to study cognitive procedural learning in early Alzheimer's disease (AD). Methods. Cognitive procedural learning was assessed using the Tower of Hanoi (TH) task. In order to take account of possible interactions between different systems during cognitive procedural learning, we also measured non‐verbal intellectual functions, working memory, and declarative memory. Results. Our results showed an apparent preservation of cognitive procedural learning in AD and a deleterious effect of the disease on verbal intelligence and declarative memory. Correlational analyses revealed a difference between AD patients and control participants in the type of processing they applied to the task. Conclusion. The non‐involvement of declarative memory would appear to be partly responsible for a slowdown in the cognitive procedural dynamics of AD patients. As the AD patients were unable to use their declarative memory, they were still in a problem‐solving mode at the end of the learning protocol and had to implement higher order cognitive processes (i.e., compensatory mechanisms) to perform the procedural task.     

情绪性记忆的定向遗忘效应

刺激的情绪性具有增强记忆的效果,那么,带有情绪信息的刺激对遗忘又会产生怎样的影响？已有研究从行为及认知神经机制层面探讨了情绪性刺激对定向遗忘效应的影响,但结果并不一致。总结已有文献发现,以情绪性刺激的材料类型、情绪效价、唤醒度和熟悉度为主的客观因素和以被试的情绪状态为主的主观因素均为影响定向遗忘效应产生及其稳定性的重要原因。这类研究是对有意遗忘研究领域的重要补充,也加深了人们对有意遗忘机制的理解。     

Arousal-Mediated Memory Consolidation: Role of the Medial TemporalLobe in Humans

Although the influence of emotional arousal on declarative memory has been documented behaviorally, the mechanisms underlying arousal-memory interactions and their representation in the human brain remain uncertain. One route through which arousal achieves its effects on memory performance is by regulating consolidation processes. Animal research has revealed that the amygdala strengthens hippocampal-dependent memory consolidation in a limited time window following participation in an arousing task. To examine whether this integrative function of amygdalo-hippocampal structures extends to the human brain, we tested unilateral-temporal-lobectomy patients on an adaptation of a classic paradigm in which levels of physiological arousal at encoding modulate retention over time. Subjects rated emotionally arousing (taboo) and neutral words on an arousal scale while their skin conductance responses (SCRs) were monitored. Recall for the words was assessed immediately and after a 1-hr delay. Both temporal-lobectomy patients and control subjects generated enhanced SCRs and arousal ratings for the arousing words at the time of encoding. However, only control subjects exhibited an increase in memory for the arousing words over time. This group difference in the effect of arousal on the rate of forgetting suggests that the role of medial temporal lobe structures in memory consolidation for arousing events is conserved across species.     

情绪记忆增强效应的时间依赖性

探讨情绪记忆短时和长时增强效应相对特异性机制以及唤醒度和效价在情绪记忆中的作用。运用不同阶段提取和不同情绪类别相结合的多因素设计方法, 对20位正常年轻成人进行行为学检测。结果显示, 情绪对记忆加工不同阶段(短时和长时)的调节作用(增强效应)具有时间依赖性, 且主要取决于情绪唤醒度, 而无显著正负效价性差异。在短时阶段主要涉及高唤醒度的增强; 而长时阶段涉及不同水平唤醒度的增强, 不同唤醒度的增强效应存在相对分离。     

The role of working memory in motor learning and performance

Three experiments explore the role of working memory in motor skill acquisition and performance. Traditional theories postulate that skill acquisition proceeds through stages of knowing, which are initially declarative but later procedural. The reported experiments challenge that view and support an independent, parallel processing model, which predicts that procedural and declarative knowledge can be acquired separately and that the former does not depend on the availability of working memory, whereas, the latter does. The behaviour of these two processes was manipulated by providing or withholding visual (and auditory) appraisal of outcome feedback. Withholding feedback was predicted to inhibit the use of working memory to appraise success and, thus, prevent the formation of declarative knowledge without affecting the accumulation of procedural knowledge. While the first experiment failed to support these predictions, the second and third experiments demonstrated that procedural and declarative knowledge can be acquired independently. It is suggested that the availability of working memory is crucial to motor performance only when the learner has come to rely on its use.     

Immediate emotion-enhanced memory dependent on arousal and valence: The role of automatic and controlled processing

The phenomenon that emotional stimuli are better remembered than neutral ones is called emotion-enhanced memory (EEM). Previous studies have shown that both valence and arousal of stimuli contributed to EEM. Kensinger and Corkin (2004) proposed that the EEM dependent on arousal was associated with automatic encoding processes, whereas the EEM dependent on valence was associated with controlled encoding processes. Their experiment with negative words provided some evidence for this associative pattern. However, it is unclear whether the observed association that occurred with negative emotional stimuli could be replicated with positive emotional stimuli. To further examine this issue, two experiments were conducted to investigate the immediate EEM of emotional words in three different attention conditions using a divided attention (DA) paradigm. Results indicated that the immediate EEM dependent on valence was associated with controlled processing, while the immediate EEM dependent on arousal was not always associated with automatic processing. The immediate EEM dependent on arousal for negative stimuli was associated with automatic processing, whereas the immediate EEM dependent on arousal for positive stimuli was associated with controlled processing. Therefore, the immediate EEM dependent on arousal, whether it is associated with automatic or controlled processing, is moderated by the valence of stimuli.     

Reconsolidation of declarative memory in humans

The reconsolidation hypothesis states that a consolidated memory could again become unstable and susceptible to facilitation or impairment for a discrete period of time after a reminder presentation. The phenomenon has been demonstrated in very diverse species and types of memory, including the human procedural memory of a motor skill task but not the human declarative one. Here we provide evidence for both consolidation and reconsolidation in a paired-associate learning (i.e., learning an association between a cue syllable and the respective response syllable). Subjects were given two training sessions with a 24-h interval on distinct verbal material, and afterward, they received at testing two successive retrievals corresponding to the first and second learning, respectively. Two main results are noted. First, the first acquired memory was impaired when a reminder was presented 5 min before the second training (reconsolidation), and also when the second training was given 5 min instead of 24 h after the first one (consolidation). Second, the first retrieval proved to influence negatively on the later one (the retrieval-induced forgetting [RIF] effect), and we used the absence of this RIF effect as a very indicator of the target memory impairment. We consider the demonstration of reconsolidation in human declarative memory as backing the universality of this phenomenon and having potential clinical relevance. On the other hand, we discuss the possibility of using the human declarative memory as a model to address several key topics of the reconsolidation hypothesis.     

What differentiates declarative and procedural memories: reply to Cohen, Poldrack, and Eichenbaum (1997)

CPE claim that procedural and declarative representations differ on two important dimensions: flexibility and compositionality. I have proposed that the apparent flexibility of a memory depends entirely on the transfer conditions. Any retest is, in some sense, a test of flexibility, because something has changed since the original encoding episodic. I have argued that if one changes something that does not provide support to memory performance, the memory will appear flexible, and resistant to changes in the environment. If one changes the very thing that the representation codes, the memory will appear inflexible and easily disrupted by changes in the environment. This principle is equally true for procedural and declarative memory. CPE contend that procedural representations lack compositionality. An ideal test of this claim would examine the representation of a task that is widely agreed to be procedural (e.g. that has been demonstrated to be learned normally by amnesic patients, and in the absence of awareness by neurologically intact subjects). Such experiments appear not to have been conducted, and the fact is that many tasks that are widely agreed to be procedural probably are not compositional. They appear to be, as CPE contend, biases in a processing system; it is hard to imagine how repetition priming could be compositional. Nevertheless, this is not true of all procedural memories. There is a good deal of evidence that motor behaviour is organised hierarchically and has compositionality. There is every reason to think that most if not all motor behaviour is procedural; motor behaviour might be driven by goals that are declarative, but the low-level operations that actually manipulate effectors are closed to consciousness, do not depend on the medial temporal lobe or diencephalon, and would therefore be classified as procedural. CPE framed their theory of differences between procedural and declarative memory systems as an account of the deficit in amnesic patients. They therefore predict that the learning of amnesic patients should not show flexibility or compositionality. There is already at least one study showing learning in amnesic patients that is as flexible as that of control participants (Knowlton & Squire, 1996). There are not, to my knowledge, data on whether the motor skill learning of amnesic patients shows compositionality, but one might expect that it would, given that it does in neurologically intact participants, and given that motor skill learning appears unimpaired in amnesic patients. Thus, the conception of declarative and procedural memory provided by CPE may not provide a complete account of amnesic performance. The anatomic distinction between procedural and declarative memory systems appears quite strong, and there is therefore reason to believe that there are accompanying computational differences. There does not, however, appear to be sufficient evidence to support those differences proposed by CPE.     

Minimizing sleep deprivation effects in healthy adults by differential outcomes

Sleep deprivation reduces vigilance or arousal levels, affecting the efficiency of certain cognitive functions such as learning and memory. Here we assessed whether the differential outcomes procedure (DOP), a learning procedure that has proved useful to ameliorate episodic memory deficits, can also improve memory performance in sleep-deprived participants. Photographs were presented as sample faces. A probe face was then presented for recognition after either short or long delays. In the differential outcomes condition a unique reinforcer followed correct responses. In the non-differential outcomes condition reinforcers were provided in a random manner. The results indicated that the DOP prevented the recognition memory to decrement during the long delay in the control group, replicating previous findings. The sleep-deprived group showed DOP benefits mainly with the short delay, when working memory could be affected by low arousal. These findings confirm that the DOP can overcome impaired recognition memory due to sleep deprivation conditions.     

Childhood amnesia and distinctions between forms of memory: A comment on Wood, Brown, and Felton

Recently, Wood and his colleagues (1989) presented a case of childhood amnesia as evidence against the distinction between declarative and procedural memory that has sometimes been applied to human amnesia. Their argument was based on the observation that their patient showed some progress in school over the years, i.e., acquired some declarative knowledge, despite severely impaired day-to-day memory ability. We briefly review their case, together with a carefully studied second case of childhood amnesia not mentioned by Wood et al. Their argument is wrong in several ways. First, the utility of the declarative/procedural distinction for amnesia, or the utility of any other distinction between memory systems, depends on whether or not one kind of memory is impaired selectively, not on the severity of the impairment. In particular there is no requirement that one kind of memory be totally absent. Second, they have not provided the data necessary to support their argument; namely, data showing that the amount of declarative knowledge accumulated during years in school was better than would have been expected given the capacity for moment-to-moment or day-to-day memory. Indeed, the patient's moment-to-moment memory ability is better than represented, and the patient's progress in school was abnormally slow. Third, it is not clear that academic achievement scores provide a direct measure of declarative memory abilities (skill learning and recovery of function may also have contributed). We conclude that the evidence from childhood amnesia is fully consistent with the proposal that amnesia reflects a selective impairment in the formation of long-term declarative memory.     

Time-limited effects of emotional arousal on item and source memory

Two experiments investigated the time-limited effects of emotional arousal on consolidation of item and source memory. In Experiment 1, participants memorized words (items) and the corresponding speakers (sources) and then took an immediate free recall test. Then they watched a neutral, positive, or negative video 5, 35, or 50?min after learning, and 24 hours later they took surprise memory tests. Experiment 2 was similar to Experiment 1 except that (a) a reality monitoring task was used; (b) elicitation delays of 5, 30, and 45?min were used; and (c) delayed memory tests were given 60?min after learning. Both experiments showed that, regardless of elicitation delay, emotional arousal did not enhance item recall memory. Second, both experiments showed that negative arousal enhanced delayed item recognition memory only at the medium elicitation delay, but not in the shorter or longer delays. Positive arousal enhanced performance only in Experiment 1. Third, regardless of elicitation delay, emotional arousal had little effect on source memory. These findings have implications for theories of emotion and memory, suggesting that emotion effects are contingent upon the nature of the memory task and elicitation delay.     

Memory dysfunction in caudate infarction caused by Heubner's recurring artery occlusion

We report five cases with caudate infarction due to Heubner's recurring artery occlusion, in which we conducted detailed memory examinations in terms of explicit memory and implicit memory. We performed the auditory verbal learning test as explicit memory tasks, and motor and cognitive procedural memory tasks, developed by Komori, as implicit memory tasks. Comparing normal control subjects with patients with left caudate infarction due to Heubner's recurring artery occlusion demonstrated lower scores on both declarative and motor procedural memory tasks. These results suggest that the left caudate nucleus may be related with both declarative memory and procedural memory.     

Role of Verbal Working Memory in Complex Skill Acquisition

Although research has shown that general cognitive ability is related to performance during the initial stage of skill acquisition, empirical evidence is needed to increase understanding of the primary abilities responsible for the relation. We propose that verbal working memory is related to initial skill acquisition performance based on cognitive activities people enact when learning complex skills. After completing a general cognitive ability measure and a test of verbal working memory, 120 undergraduate students performed a complex computer simulation. The working memory test accounted for a meaningful amount of performance variance after statistically controlling for the general cognitive ability measure. These data suggest that tasks depending heavily on the activation of multiple knowledge structures may be understood in terms of individual differences in working memory.     

Immediate memory consequences of the effect of emotion on attention to pictures

Emotionally arousing stimuli are at once both highly attention grabbing and memorable. We examined whether emotional enhancement of memory (EEM) reflects an indirect effect of emotion on memory, mediated by enhanced attention to emotional items during encoding. We tested a critical prediction of the mediation hypothesis-that regions conjointly activated by emotion and attention would correlate with subsequent EEM. Participants were scanned with fMRI while they watched emotional or neutral pictures under instructions to attend to them a lot or a little, and were then given an immediate recognition test. A region in the left fusiform gyrus was activated by emotion, voluntary attention, and subsequent EEM. A functional network, different for each attention condition, connected this region and the amygdala, which was associated with emotion and EEM, but not with voluntary attention. These findings support an indirect cortical mediation account of immediate EEM that may complement a direct modulation model.     

When can we choose to forget? An ERP study into item-method directed forgetting of emotional words

Emotionally arousing information is treated in a specialised manner across a number of different processing stages, and memory for affective events is often found to be heightened by virtue of this. However, in some cases, emotional experiences might be the very ones that we would like to forget. Here, two item-method directed forgetting studies are presented which investigate people's ability to intentionally forget affective words when stimuli and memory instructions are presented simultaneously. In the first experiment an interaction between task instruction and emotional content was evident in a diminished directed forgetting effect for emotional words, suggesting that they may be relatively resistant to deliberate forgetting. The interaction between instruction and emotion appeared both in free recall of words and in a yes-no recognition task. In the second study, an ERP procedure was utilised to investigate whether emotion modulates the effects of instruction during the initial encoding of stimuli. Recognition data again showed a clear interaction between instruction and emotion, with a reduced directed forgetting effect for emotional words. The ERP data demonstrated evidence for individual effects of both emotion and instruction during encoding; however, despite this, no evidence for an interaction between these factors was evident in the ERP data. As such, we conclude that even when study items are presented simultaneously with their associated memory instructions, neither does emotion prevent differential processing of directed forgetting instruction, nor does memory instruction prevent differential processing of emotion during early encoding. Implications are discussed in relation to the directed forgetting literature and more broadly with respect to circumstances under which emotion and cognitive processing work in parallel or in competition with each other.