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.     

The contribution of sleep to hippocampus-dependent memory consolidation

There is now compelling evidence that sleep promotes the long-term consolidation of declarative and procedural memories. Behavioral studies suggest that sleep preferentially consolidates explicit aspects of these memories, which during encoding are possibly associated with activation in prefrontal-hippocampal circuitry. Hippocampus-dependent declarative memory benefits particularly from slow-wave sleep (SWS), whereas rapid-eye-movement (REM) sleep seems to benefit procedural aspects of memory. Consolidation of hippocampus-dependent memories relies on a dialog between the neocortex and hippocampus. Crucial features of this dialog are the neuronal reactivation of new memories in the hippocampus during SWS, which stimulates the redistribution of memory representations to neocortical networks; and the neocortical slow (<1Hz) oscillation that synchronizes hippocampal-to-neocortical information transfer to activity in other brain structures.     

Processing of representations in declarative and procedural working memory

The article investigates the relation between declarative and procedural working memory (WM; Oberauer, 2009). Two experiments test the assumption that representations in the two subsystems are selected for processing in analogous ways. Participants carried out a series of decisions on memorized lists of digits. For each decision, they had to select declarative and procedural representations. Regarding declarative representations, participants selected a memory set and a digit within this set as the input to each decision. With respect to the procedural representations, they selected a task set to be applied to the selected digit and a response within that task set. We independently manipulated the number of lists and the number of tasks to be switched among (one, two, or three; Experiment 1) and preparation time for a list switch (Experiment 2). For three effects commonly observed in task-switch studies, analogues in declarative WM were found: list-switch costs, mixing costs, and residual switch costs. List- and task-switch costs were underadditive, suggesting that declarative and procedural representations are selected separately and in parallel. The findings support the hypothesis of two analogous WM subsystems.     

Processing of representations in declarative and procedural working memory

The article investigates the relation between declarative and procedural working memory (WM; Oberauer, 2009). Two experiments test the assumption that representations in the two subsystems are selected for processing in analogous ways. Participants carried out a series of decisions on memorized lists of digits. For each decision, they had to select declarative and procedural representations. Regarding declarative representations, participants selected a memory set and a digit within this set as the input to each decision. With respect to the procedural representations, they selected a task set to be applied to the selected digit and a response within that task set. We independently manipulated the number of lists and the number of tasks to be switched among (one, two, or three; Experiment 1) and preparation time for a list switch (Experiment 2). For three effects commonly observed in task-switch studies, analogues in declarative WM were found: list-switch costs, mixing costs, and residual switch costs. List- and task-switch costs were underadditive, suggesting that declarative and procedural representations are selected separately and in parallel. The findings support the hypothesis of two analogous WM subsystems.     

Reactivation and Consolidation of Memory During Sleep

ABSTRACT— Recent research has shown compellingly that sleep supports the consolidation of declarative memories for events and facts. During consolidation, memories are stabilized against future interference and undergo qualitative changes with regard to their "explicitness" and underlying neural representation. In this article, we argue that declarative memory consolidation during sleep is based on covert reactivations of newly encoded memory traces in the hippocampus. During slow-wave sleep (SWS), the prominent slow oscillations act to synchronize the repeated reactivation of the newly encoded representations in hippocampal networks with the generation of spindle activity in the thalamus, supporting changes in neocortical networks that contribute to long-term memory storage. In this view, sleep plays an active role in the consolidation of memories, in which the neuronal reactivation of newly acquired memories is critical for the redistribution and integration of these memories into the network of pre-existing long-term memories.     

Mechanisms of change: exploring not only when and what,but also how declarative memory develops

Age‐related changes in representational flexibility are a characteristic feature of declarative memory development. The authors suggest that a qualitative shift in the nature of infants' memory representations accounts for increasing memory flexibility with age. We will argue that a comprehensive theory of declarative memory development must (1) account for the effect of experience on flexibility, (2) be empirically separable from more parsimonious explanations, and (3) propose a mechanism by which the transition takes place. We will argue that a converging‐methods approach is necessary to understand not only when and what develops in declarative memory, but also how developmental change occurs. Copyright © 2006 John Wiley & Sons, Ltd.     

Long-term follow-up of a childhood amnesic syndrome

In attempting to explain observed dissociations between impaired and preserved memory functioning in amnesia, various dichotomous memory systems (e.g., procedural versus declarative, episodic versus semantic, working versus reference memory) have often been employed. In such cases, the assumption has been that memory subserved by one system is preserved, while that of the other system is impaired. Cohen and Squire have suggested that in amnesia, declarative memory is impaired, although procedural memory is preserved. Long-term follow-up of a densely amnesic patient refutes this view by demonstrating significant anterograde learning of school subjects including reading, vocabulary, spelling, and arithmetic, all of which include some component of declarative memory. It appears that the procedural/declarative dichotomy is not adequate to explain preserved memory in amnesia.     

Analogous selection processes in declarative and procedural working memory: N-2 list-repetition and task-repetition costs

Working memory (WM) holds and manipulates representations for ongoing cognition. Oberauer (Psychology of Learning and Motivation, 51, 45–100, 2009) distinguishes between two analogous WM sub-systems: a declarative WM which handles the objects of thought, and a procedural WM which handles the representations of (cognitive) actions. Here, we assessed whether analogous effects are observed when participants switch between memory sets (declarative representations) and when they switch between task sets (procedural representations). One mechanism assumed to facilitate switching in procedural WM is the inhibition of previously used, but currently irrelevant task sets, as indexed by n-2 task-repetition costs (Mayr & Keele, Journal of Experimental Psychology: General, 129(1), 4–26, 2000). In this study we tested for an analogous effect in declarative WM. We assessed the evidence for n-2 list-repetition costs across eight experiments in which participants switched between memory lists to perform speeded classifications, mental arithmetic, or a local recognition test. N-2 list-repetition costs were obtained consistently in conditions assumed to increase interference between memory lists, and when lists formed chunks in long-term memory. Further analyses across experiments revealed a substantial contribution of episodic memory to n-2 list-repetition costs, thereby questioning the interpretation of n-2 repetition costs as reflecting inhibition. We reanalyzed the data of eight task-switching experiments, and observed that episodic memory also contributes to n-2 task-repetition costs. Taken together, these results show analogous processing principles in declarative and procedural WM, and question the relevance of inhibitory processes for efficient switching between mental sets.     

Memory systems and the control of skilled action

ABSTRACT

In keeping with the dominant view that skills are largely automatic, the standard view of memory systems distinguishes between a representational declarative system associated with cognitive processes and a performance-based procedural system. The procedural system is thought to be largely responsible for the performance of well-learned skilled actions. Here we argue that most skills do not fully automate, which entails that the declarative system should make a substantial contribution to skilled performance. To support this view, we review evidence showing that the declarative system does indeed play a number of roles in skilled action.     

Analogous mechanisms of selection and updating in declarative and procedural working memory: Experiments and a computational model

The article investigates the mechanisms of selecting and updating representations in declarative and procedural working memory (WM). Declarative WM holds the objects of thought available, whereas procedural WM holds representations of what to do with these objects. Both systems consist of three embedded components: activated long-term memory, a central capacity-limited component for building structures through temporary bindings, and a single-element focus of attention. Five experiments test the hypothesis of analogous mechanisms in declarative and procedural WM, investigating repetition effects across trials for individual representations (objects and responses) and for sets (memory sets and task sets), as well as set-congruency effects. Evidence for analogous processes was obtained from three phenomena: (1) Costs of task switching and of list switching are reduced with longer preparation interval. (2) The effects of task congruency and of list congruency are undiminished with longer preparation interval. (3) Response repetition interacts with task repetition in procedural WM; here we show an analogous interaction of list repetition with item repetition in declarative WM. All three patterns were reproduced by a connectionist model implementing the assumed selection and updating mechanisms. The model consists of two modules, an item-selection module selecting individual items from a memory set, or responses from a task set, and a set-selection module for selecting memory sets or task sets. The model codes the matrix of binding weights in the item-selection module as a pattern of activation in the set-selection module, thereby providing a mechanism for building chunks in LTM, and for unpacking them as structures into working memory.     

Exploring memory in infancy: deferred imitation and the development of declarative memory

Imitation is an important means by which infants learn new behaviours. When infants do not have the opportunity to immediately reproduce observed actions, they may form a memory representation of the event which can guide their behaviour when a similar situation is encountered again. Imitation procedures can, therefore, provide insight into infant memory. The deferred imitation paradigm requires a modelled action to be reproduced following a delay, without prior motor practice. As such, deferred imitation procedures have been proposed to tap declarative memory abilities in non‐verbal populations such as infants. Contrary to the popular belief that infants form sparse or ill‐defined memories, deferred imitation research reveals that infants store and retrieve highly detailed memory representations. The specificity of detail encoded into the representation can, however, cause memory retrieval to fail at young ages. Developing the ability to identify event components which are central (the target stimulus) versus details which are peripheral (the exact context in which learning occurred) is therefore an important aspect of memory development. Using deferred imitation procedures to study the transition from constrained to flexible memory representations can thus facilitate our understanding of the development of declarative memory during the infancy period. Copyright © 2006 John Wiley & Sons, Ltd.     

System consolidation of memory during sleep

Over the past two decades, research has accumulated compelling evidence that sleep supports the formation of long-term memory. The standard two-stage memory model that has been originally elaborated for declarative memory assumes that new memories are transiently encoded into a temporary store (represented by the hippocampus in the declarative memory system) before they are gradually transferred into a long-term store (mainly represented by the neocortex), or are forgotten. Based on this model, we propose that sleep, as an offline mode of brain processing, serves the ‘active system consolidation’ of memory, i.e. the process in which newly encoded memory representations become redistributed to other neuron networks serving as long-term store. System consolidation takes place during slow-wave sleep (SWS) rather than rapid eye movement (REM) sleep. The concept of active system consolidation during sleep implicates that (a) memories are reactivated during sleep to be consolidated, (b) the consolidation process during sleep is selective inasmuch as it does not enhance every memory, and (c) memories, when transferred to the long-term store undergo qualitative changes. Experimental evidence for these three central implications is provided: It has been shown that reactivation of memories during SWS plays a causal role for consolidation, that sleep and specifically SWS consolidates preferentially memories with relevance for future plans, and that sleep produces qualitative changes in memory representations such that the extraction of explicit and conscious knowledge from implicitly learned materials is facilitated.     

Reinstatement of odour context cues veridical memories but not false memories

ABSTRACT

The sense of smell has made a recent return to the forefront of research on episodic memory. Odour context cues can reactivate recently encoded memories during sleep-dependent memory consolidation [e.g., Rasch, B., Buchel, C., Gais, S., & Born, J. (2007). Odor cues during slow-wave sleep prompt declarative memory consolidation. Science, 315, 1426–1429], and reinstating the odour experienced during encoding at test results in superior recall and recognition [e.g., Isarida, T., Sakai, T., Kubota, T., Koga, M., Katayama, Y., & Isarida, T. K. (2014). Odor-context effects in free recall after a short retention interval: A new methodology for controlling adaptation. Memory & Cognition, 42, 421–433]. However, whether the impact of odour cues is restricted to the specific memories studied in the presence of the odour, or whether reinstating the odour also cues unstudied memories that are semantically related to the studied memories (i.e., false memories) is unknown. We used the Deese-Roediger-McDermott false memory paradigm to quantify the impact of odour cues on both veridical memory and false memory. Reinstating the odour presented during the study of the DRM word lists at the test phase resulted in better free recall of the studied words, but had no statistically significant impact on the number of false memories produced. We argue that odour cues influence recall of the memories they co-occurred with during study but potentially not semantically related memories.     

Memory reactivation and consolidation during sleep

Do our memories remain static during sleep, or do they change? We argue here that memory change is not only a natural result of sleep cognition, but further, that such change constitutes a fundamental characteristic of declarative memories. In general, declarative memories change due to retrieval events at various times after initial learning and due to the formation and elaboration of associations with other memories, including memories formed after the initial learning episode. We propose that declarative memories change both during waking and during sleep, and that such change contributes to enhancing binding of the distinct representational components of some memories, and thus to a gradual process of cross-cortical consolidation. As a result of this special form of consolidation, declarative memories can become more cohesive and also more thoroughly integrated with other stored information. Further benefits of this memory reprocessing can include developing complex networks of interrelated memories, aligning memories with long-term strategies and goals, and generating insights based on novel combinations of memory fragments. A variety of research findings are consistent with the hypothesis that cross-cortical consolidation can progress during sleep, although further support is needed, and we suggest some potentially fruitful research directions. Determining how processing during sleep can facilitate memory storage will be an exciting focus of research in the coming years.The idea that memory storage is supported by events that take place in the brain while a person is sleeping is an idea that is only rarely acknowledged in the neuroscience community. At present, most memory research proceeds with no mention of any influence of sleep on memory. Nonetheless, this hypothesis is gaining empirical support. Research into connections between memory and sleep represents a burgeoning enterprise at the crossroads of traditional memory research and sleep research, an enterprise poised to provide novel insights into the human experience.This article presents some speculations about connections between memory and sleep. We entertain the notion that declarative memories are subject to modification during sleep, and that enduring storage of such memories is systematically influenced by neural events taking place during sleep. Although other types of memory may also be subject to change during sleep (see Maquet et al. 2003), we emphasize declarative memory here.This article also functions as an introduction to the set of papers selected for this special issue of Learning & Memory. These papers together outline portions of the current empirical basis for memory-sleep connections, including research in humans and in nonhuman animals. The findings are tantalizing, and yet there are undoubtedly major gaps in our knowledge about the functions of sleep and about how sleep may be related to memory storage. Future research on this topic is bound to grow in exciting and unpredictable ways. Here, we explore questions about declarative memory and sleep that may serve as a useful guide for such research.     

Longitudinal study of declarative and procedural memory in primary school‐aged children

This study examined the development of declarative and procedural memory longitudinally in primary school‐aged children. At present, although there is a general consensus that age‐related improvements during this period can be found for declarative memory, there are conflicting data on the developmental trajectory of the procedural memory system. At Time 1 children aged around 5½ years were presented with measures of declarative and procedural memory. The tasks were then administered 12 months later. Performance on the declarative memory task was found to improve at a faster rate in comparison to the procedural memory task. The findings of the study support the view that multiple memory systems reach functional maturity at different points in development.     

Memory consolidation during sleep: interactive effects of sleep stages and HPA regulation

Sleep is critically involved in the consolidation of previously acquired memory traces. However, nocturnal sleep is not uniform but is subject to distinct changes in electrophysiological and neuroendocrine activity. Specifically, the first half of the night is dominated by slow wave sleep (SWS), whereas rapid eye movement (REM) sleep prevails in the second half. Concomitantly, hypothalamo-pituitary-adrenal (HPA) activity as indicated by cortisol release is suppressed to a minimum during early sleep, while drastically increasing during late sleep. We have shown that the different sleep stages and the concomitant glucocorticoid release are interactively involved in the consolidation of different types of memories. SWS-rich early sleep has been demonstrated to benefit mainly the consolidation of hippocampus-dependent declarative memories (i.e. facts and episodes). In contrast, REM sleep-rich late sleep was shown to improve in particular emotional memories involving amygdalar function, as well as procedural memories (for skills) not depending on hippocampal or amygdalar function. Enhancing plasma glucocorticoid concentrations during SWS-rich early sleep counteracted hippocampus-dependent declarative memory consolidation, but did not affect hippocampus-independent procedural memory. Preventing the increase in cortisol during late REM sleep-rich sleep by administration of metyrapone impaired hippocampus-dependent declarative memory but enhanced amygdala-dependent emotional aspects of memory. The data underscore the importance of pituitary-adrenal inhibition during early SWS-rich sleep for efficient consolidation of declarative memory. The increase in cortisol release during late REM sleep-rich sleep may counteract an overshooting consolidation of emotional memories.     

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.     

原发性失眠对睡眠依赖性记忆巩固的影响及机制

现代社会的失眠问题异常突出,其对睡眠依赖性记忆巩固（SDC）的影响日益引起重视。目前,原发性失眠（PI）对陈述性及程序性记忆SDC的影响存在分歧。梳理以往研究发现,系统巩固假说和突触稳态假说支持睡眠结构紊乱及脑结构异常可能是PI患者SDC损伤的潜在脑机制。未来研究可考虑同步采集行为、脑电和脑成像数据,深入探究PI影响SDC的脑机制,并验证上述假说;还可尝试通过经颅电/磁刺激和目标记忆重激活等无创性干预措施改善PI患者的SDC效应。     

Declarative strategies persist under increased cognitive load

When humans simultaneously execute multiple tasks, performance on individual tasks suffers. Complementing existing theories, this article poses a novel question to investigate interactions between memory systems supporting multi-tasking performance: When a primary and dual task both recruit declarative learning and memory systems, does simultaneous performance of both tasks impair primary task performance because learning in the declarative system is reduced, or because control of the primary task is passed to slower procedural systems? To address this question, participants were trained on either a perceptual categorization task believed to rely on procedural learning or one of three different categorization tasks believed to rely on declarative learning. Task performance was examined with and without a simultaneous dual task thought to recruit working memory and executive attention. To test whether the categories were learned procedurally or declaratively, the response keys were switched after a learning criterion had been reached. Large impairments in performance after switching the response keys are taken to indicate procedural learning, and small impairments are taken to indicate declarative learning. Our results suggest that the declarative memory categorization tasks (regardless of task difficulty) were learned by declarative systems, regardless of whether they were learned under dual-task 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.