Delayed Onset of a Daytime Nap Facilitates Retention of Declarative Memory

Background

Learning followed by a period of sleep, even as little as a nap, promotes memory consolidation. It is now generally recognized that sleep facilitates the stabilization of information acquired prior to sleep. However, the temporal nature of the effect of sleep on retention of declarative memory is yet to be understood. We examined the impact of a delayed nap onset on the recognition of neutral pictorial stimuli with an added spatial component.

Methodology/Principal Findings

Participants completed an initial study session involving 150 neutral pictures of people, places, and objects. Immediately following the picture presentation, participants were asked to make recognition judgments on a subset of “old”, previously seen, pictures versus intermixed “new” pictures. Participants were then divided into one of four groups who either took a 90-minute nap immediately, 2 hours, or 4 hours after learning, or remained awake for the duration of the experiment. 6 hours after initial learning, participants were again tested on the remaining “old” pictures, with “new” pictures intermixed.

Conclusions/Significance

Interestingly, we found a stabilizing benefit of sleep on the memory trace reflected as a significant negative correlation between the average time elapsed before napping and decline in performance from test to retest (p = .001). We found a significant interaction between the groups and their performance from test to retest (p = .010), with the 4-hour delay group performing significantly better than both those who slept immediately and those who remained awake (p = .044, p = .010, respectively). Analysis of sleep data revealed a significant positive correlation between amount of slow wave sleep (SWS) achieved and length of the delay before sleep onset (p = .048). The findings add to the understanding of memory processing in humans, suggesting that factors such as waking processing and homeostatic increases in need for sleep over time modulate the importance of sleep to consolidation of neutral declarative memories.     

Relationship between Fear Conditionability and Aversive Memories: Evidence from a Novel Conditioned-Intrusion Paradigm

Intrusive memories – a hallmark symptom of posttraumatic stress disorder (PTSD) – are often triggered by stimuli possessing similarity with cues that predicted or accompanied the traumatic event. According to learning theories, intrusive memories can be seen as a conditioned response to trauma reminders. However, direct laboratory evidence for the link between fear conditionability and intrusive memories is missing. Furthermore, fear conditioning studies have predominantly relied on standardized aversive stimuli (e.g. electric stimulation) that bear little resemblance to typical traumatic events. To investigate the general relationship between fear conditionability and aversive memories, we tested 66 mentally healthy females in a novel conditioned-intrusion paradigm designed to model real-life traumatic experiences. The paradigm included a differential fear conditioning procedure with neutral sounds as conditioned stimuli and short violent film clips as unconditioned stimuli. Subsequent aversive memories were assessed through a memory triggering task (within 30 minutes, in the laboratory) and ambulatory assessment (involuntary aversive memories in the 2 days following the experiment). Skin conductance responses and subjective ratings demonstrated successful differential conditioning indicating that naturalistic aversive film stimuli can be used in a fear conditioning experiment. Furthermore, aversive memories were elicited in response to the conditioned stimuli during the memory triggering task and also occurred in the 2 days following the experiment. Importantly, participants who displayed higher conditionability showed more aversive memories during the memory triggering task and during ambulatory assessment. This suggests that fear conditioning constitutes an important source of persistent aversive memories. Implications for PTSD and its treatment are discussed.     

Interaction of Sleep and Emotional Content on the Production of False Memories

Sleep benefits veridical memories, resulting in superior recall relative to off-line intervals spent awake. Sleep also increases false memory recall in the Deese-Roediger-McDermott (DRM) paradigm. Given the suggestion that emotional veridical memories are prioritized for consolidation over sleep, here we examined whether emotion modulates sleep’s effect on false memory formation. Participants listened to semantically related word lists lacking a critical lure representing each list’s “gist.” Free recall was tested after 12 hours containing sleep or wake. The Sleep group recalled more studied words than the Wake group but only for emotionally neutral lists. False memories of both negative and neutral critical lures were greater following sleep relative to wake. Morning and Evening control groups (20-minute delay) did not differ ruling out circadian accounts for these differences. These results support the adaptive function of sleep in both promoting the consolidation of veridical declarative memories and in extracting unifying aspects from memory details.     

Applying an Attentional Set to Perceived and Remembered Features

Previous research has examined our ability to attend selectively to particular features of perceptual objects, as well as our ability to switch from attending to one type of feature to another. This is usually done in the context of anticipatory attentional-set control, comparing the neural mechanisms involved as participants prepare to attend to the same stimulus feature as on the previous trial (“task-stay” trials) with those required as participants prepare to attend to a different stimulus feature to that previously attended (“task-switch” trials). We wanted to establish how participants maintain or switch attentional set retrospectively, as they attend to features of objects held in visual short-term memory (VSTM). We found that switching, relative to maintaining attentional set retrospectively, was associated with a performance cost, which can be reduced over time. This control process was mirrored by a large parietal and frontal amplitude difference in the event-related brain potentials (ERPs) and significant differences in global field power (GFP) between switch and stay trials. However, when taking into account the switch/stay GFP differences, thereby controlling for this difference in amplitude, we could not distinguish these trial types topographically. By contrast, we found clear topographic differences between preparing an anticipatory feature-based attentional set versus applying it retrospectively within VSTM. These complementary topographical and amplitude analyses suggested that anticipatory and retrospective set control recruited a qualitatively different configuration of underlying neural generators. In contrast, switch/stay differences were largely quantitative, with them differing primarily in terms of amplitude rather than topography.     

The Roles of Noradrenergic and Glucocorticoid Activation in the Development of Intrusive Memories

Intrusive memories are a common feature of many psychological disorders. Recent evidence has potentially extended cognitive models of intrusions by identifying the role of biological markers of arousal at the time of consolidation in subsequent memory for emotional events. This study investigated the role of arousal during consolidation in the development of intrusive memories. Seventy-eight university students (37 men and 41 women) viewed 20 negative and 20 neutral images. Half the participants then underwent a cold pressor test (High Stress), immersing their hand in ice water, while the remaining participants immersed their hand in warm water (Low Stress). Samples of salivary alpha-amylase (sAA) and cortisol were collected from participants at baseline and following the stressor challenge. Participants completed a delayed free recall test and intrusion questionnaires two days later. Participants in the High Stress condition reported more intrusions of negative images than participants in the Low Stress condition. An interaction variable in a linear regression of increased noradrenergic and cortisol values predicted intrusive memories of emotional stimuli for men but not women. These findings are consistent with recent evidence of the combined effects of noradrenaline and corticoid responses to stress on emotional memories, and also with increasing evidence of gender differences in how stress hormones influence formation of emotional memories. These findings point to possible mechanisms by which development of intrusions may be prevented after consolidation of traumatic experiences.     

The Impact of Social Context and Language Comprehension on Behaviour: A Kinematic Investigation

We investigated whether and how comprehending sentences that describe a social context influences our motor behaviour. Our stimuli were sentences that referred to objects having different connotations (e.g., attractive/ugly vs. smooth/prickly) and that could be directed towards the self or towards “another person” target (e.g., “The object is ugly/smooth. Bring it to you/Give it to another person”). Participants judged whether each sentence was sensible or non-sensible by moving the mouse towards or away from their body. Mouse movements were analysed according to behavioral and kinematics parameters. In order to enhance the social meaning of the linguistic stimuli, participants performed the task either individually (Individual condition) or in a social setting, in co-presence with the experimenter. The experimenter could either act as a mere observer (Social condition) or as a confederate, interacting with participants in an off-line modality at the end of task execution (Joint condition). Results indicated that the different roles taken by the experimenter affected motor behaviour and are discussed within an embodied approach to language processing and joint actions.     

Modeling spatial–temporal operations with context-dependent associative memories

We organize our behavior and store structured information with many procedures that require the coding of spatial and temporal order in specific neural modules. In the simplest cases, spatial and temporal relations are condensed in prepositions like “below” and “above”, “behind” and “in front of”, or “before” and “after”, etc. Neural operators lie beneath these words, sharing some similarities with logical gates that compute spatial and temporal asymmetric relations. We show how these operators can be modeled by means of neural matrix memories acting on Kronecker tensor products of vectors. The complexity of these memories is further enhanced by their ability to store episodes unfolding in space and time. How does the brain scale up from the raw plasticity of contingent episodic memories to the apparent stable connectivity of large neural networks? We clarify this transition by analyzing a model that flexibly codes episodic spatial and temporal structures into contextual markers capable of linking different memory modules.     

Within- and Cross-Modal Distance Information Disambiguate Visual Size-Change Perception

Perception is fundamentally underconstrained because different combinations of object properties can generate the same sensory information. To disambiguate sensory information into estimates of scene properties, our brains incorporate prior knowledge and additional “auxiliary” (i.e., not directly relevant to desired scene property) sensory information to constrain perceptual interpretations. For example, knowing the distance to an object helps in perceiving its size. The literature contains few demonstrations of the use of prior knowledge and auxiliary information in combined visual and haptic disambiguation and almost no examination of haptic disambiguation of vision beyond “bistable” stimuli. Previous studies have reported humans integrate multiple unambiguous sensations to perceive single, continuous object properties, like size or position. Here we test whether humans use visual and haptic information, individually and jointly, to disambiguate size from distance. We presented participants with a ball moving in depth with a changing diameter. Because no unambiguous distance information is available under monocular viewing, participants rely on prior assumptions about the ball''s distance to disambiguate their -size percept. Presenting auxiliary binocular and/or haptic distance information augments participants'' prior distance assumptions and improves their size judgment accuracy—though binocular cues were trusted more than haptic. Our results suggest both visual and haptic distance information disambiguate size perception, and we interpret these results in the context of probabilistic perceptual reasoning.     

The Visual Priming of Motion-Defined 3D Objects

The perception of a stimulus can be influenced by previous perceptual experience, a phenomenon known as perceptual priming. However, there has been limited investigation on perceptual priming of shape perception of three-dimensional object structures defined by moving dots. Here we examined the perceptual priming of a 3D object shape defined purely by motion-in-depth cues (i.e., Shape-From-Motion, SFM) using a classic prime-target paradigm. The results from the first two experiments revealed a significant increase in accuracy when a “cloudy” SFM stimulus (whose object structure was difficult to recognize due to the presence of strong noise) was preceded by an unambiguous SFM that clearly defined the same transparent 3D shape. In contrast, results from Experiment 3 revealed no change in accuracy when a “cloudy” SFM stimulus was preceded by a static shape or a semantic word that defined the same object shape. Instead, there was a significant decrease in accuracy when preceded by a static shape or a semantic word that defined a different object shape. These results suggested that the perception of a noisy SFM stimulus can be facilitated by a preceding unambiguous SFM stimulus—but not a static image or a semantic stimulus—that defined the same shape. The potential neural and computational mechanisms underlying the difference in priming are discussed.     

Probability Matching as a Computational Strategy Used in Perception

The question of which strategy is employed in human decision making has been studied extensively in the context of cognitive tasks; however, this question has not been investigated systematically in the context of perceptual tasks. The goal of this study was to gain insight into the decision-making strategy used by human observers in a low-level perceptual task. Data from more than 100 individuals who participated in an auditory-visual spatial localization task was evaluated to examine which of three plausible strategies could account for each observer''s behavior the best. This task is very suitable for exploring this question because it involves an implicit inference about whether the auditory and visual stimuli were caused by the same object or independent objects, and provides different strategies of how using the inference about causes can lead to distinctly different spatial estimates and response patterns. For example, employing the commonly used cost function of minimizing the mean squared error of spatial estimates would result in a weighted averaging of estimates corresponding to different causal structures. A strategy that would minimize the error in the inferred causal structure would result in the selection of the most likely causal structure and sticking with it in the subsequent inference of location—“model selection.” A third strategy is one that selects a causal structure in proportion to its probability, thus attempting to match the probability of the inferred causal structure. This type of probability matching strategy has been reported to be used by participants predominantly in cognitive tasks. Comparing these three strategies, the behavior of the vast majority of observers in this perceptual task was most consistent with probability matching. While this appears to be a suboptimal strategy and hence a surprising choice for the perceptual system to adopt, we discuss potential advantages of such a strategy for perception.     

Be Happy Not Sad for Your Youth: The Effect of Emotional Expression on Age Perception

Perceived age is a psychosocial factor that can influence both with whom and how we choose to interact socially. Though intuition tells us that a smile makes us look younger, surprisingly little empirical evidence exists to explain how age-irrelevant emotional expressions bias the subjective decision threshold for age. We examined the role that emotional expression plays in the process of judging one’s age from a face. College-aged participants were asked to sort the emotional and neutral expressions of male facial stimuli that had been morphed across eight age levels into categories of either “young” or “old.” Our results indicated that faces at the lower age levels were more likely to be categorized as old when they showed a sad facial expression compared to neutral expressions. Mirroring that, happy faces were more often judged as young at higher age levels than neutral faces. Our findings suggest that emotion interacts with age perception such that happy expression increases the threshold for an old decision, while sad expression decreases the threshold for an old decision in a young adult sample.     

Eye Tracking,Cortisol, and a Sleep vs. Wake Consolidation Delay: Combining Methods to Uncover an Interactive Effect of Sleep and Cortisol on Memory

Although rises in cortisol can benefit memory consolidation, as can sleep soon after encoding, there is currently a paucity of literature as to how these two factors may interact to influence consolidation. Here we present a protocol to examine the interactive influence of cortisol and sleep on memory consolidation, by combining three methods: eye tracking, salivary cortisol analysis, and behavioral memory testing across sleep and wake delays. To assess resting cortisol levels, participants gave a saliva sample before viewing negative and neutral objects within scenes. To measure overt attention, participants’ eye gaze was tracked during encoding. To manipulate whether sleep occurred during the consolidation window, participants either encoded scenes in the evening, slept overnight, and took a recognition test the next morning, or encoded scenes in the morning and remained awake during a comparably long retention interval. Additional control groups were tested after a 20 min delay in the morning or evening, to control for time-of-day effects. Together, results showed that there is a direct relation between resting cortisol at encoding and subsequent memory, only following a period of sleep. Through eye tracking, it was further determined that for negative stimuli, this beneficial effect of cortisol on subsequent memory may be due to cortisol strengthening the relation between where participants look during encoding and what they are later able to remember. Overall, results obtained by a combination of these methods uncovered an interactive effect of sleep and cortisol on memory consolidation.     

MM-MDS: A Multidimensional Scaling Database with Similarity Ratings for 240 Object Categories from the Massive Memory Picture Database

Cognitive theories in visual attention and perception, categorization, and memory often critically rely on concepts of similarity among objects, and empirically require measures of “sameness” among their stimuli. For instance, a researcher may require similarity estimates among multiple exemplars of a target category in visual search, or targets and lures in recognition memory. Quantifying similarity, however, is challenging when everyday items are the desired stimulus set, particularly when researchers require several different pictures from the same category. In this article, we document a new multidimensional scaling database with similarity ratings for 240 categories, each containing color photographs of 16–17 exemplar objects. We collected similarity ratings using the spatial arrangement method. Reports include: the multidimensional scaling solutions for each category, up to five dimensions, stress and fit measures, coordinate locations for each stimulus, and two new classifications. For each picture, we categorized the item''s prototypicality, indexed by its proximity to other items in the space. We also classified pairs of images along a continuum of similarity, by assessing the overall arrangement of each MDS space. These similarity ratings will be useful to any researcher that wishes to control the similarity of experimental stimuli according to an objective quantification of “sameness.”     

Plant intelligence: Why,why not or where?

The concept of plant intelligence, as proposed by Anthony Trewavas, has raised considerable discussion. However, plant intelligence remains loosely defined; often it is either perceived as practically synonymous to Darwinian fitness, or reduced to a mere decorative metaphor. A more strict view can be taken, emphasizing necessary prerequisites such as memory and learning, which requires clarifying the definition of memory itself. To qualify as memories, traces of past events have to be not only stored, but also actively accessed. We propose a criterion for eliminating false candidates of possible plant intelligence phenomena in this stricter sense: an “intelligent” behavior must involve a component that can be approximated by a plausible algorithmic model involving recourse to stored information about past states of the individual or its environment. Re-evaluation of previously presented examples of plant intelligence shows that only some of them pass our test.

“You were hurt?” Kumiko said, looking at the scar.Sally looked down. “Yeah.”“Why didn''t you have it removed?”“Sometimes it''s good to remember.”“Being hurt?”“Being stupid.”—(W. Gibson: Mona Lisa Overdrive)

Key words: intelligence, memory, learning, plant development, mathematical models, plant neurobiology, definition of terms     

Viewing Complex,Dynamic Scenes “Through the Eyes” of Another Person: The Gaze-Replay Paradigm

We present a novel “Gaze-Replay” paradigm that allows the experimenter to directly test how particular patterns of visual input—generated from people’s actual gaze patterns—influence the interpretation of the visual scene. Although this paradigm can potentially be applied across domains, here we applied it specifically to social comprehension. Participants viewed complex, dynamic scenes through a small window displaying only the foveal gaze pattern of a gaze “donor.” This was intended to simulate the donor’s visual selection, such that a participant could effectively view scenes “through the eyes” of another person. Throughout the presentation of scenes presented in this manner, participants completed a social comprehension task, assessing their abilities to recognize complex emotions. The primary aim of the study was to assess the viability of this novel approach by examining whether these Gaze-Replay windowed stimuli contain sufficient and meaningful social information for the viewer to complete this social perceptual and cognitive task. The results of the study suggested this to be the case; participants performed better in the Gaze-Replay condition compared to a temporally disrupted control condition, and compared to when they were provided with no visual input. This approach has great future potential for the exploration of experimental questions aiming to unpack the relationship between visual selection, perception, and cognition.     

A Puzzle Unsolved: Failure to Observe Different Effects of God and Religion Primes on Intergroup Attitudes

Religious priming has been found to have both positive and negative consequences, and recent research suggests that the activation of God-related and community-related religious cognitions may cause outgroup prosociality and outgroup derogation respectively. The present research sought to examine whether reminders of God and religion have different effects on attitudes towards ingroup and outgroup members. Over two studies, little evidence was found for different effects of these two types of religious primes. In study 1, individuals primed with the words “religion”, “God” and a neutral control word evaluated both ingroup and outgroup members similarly, although a marginal tendency towards more negative evaluations of outgroup members by females exposed to religion primes was observed. In study 2, no significant differences in attitudes towards an outgroup member were observed between the God, religion, and neutral priming conditions. Furthermore, the gender effect observed in study 1 did not replicate in this second study. Possible explanations for these null effects are discussed.     

Does Recall after Sleep-Dependent Memory Consolidation Reinstate Sensitivity to Retroactive Interference?

Previous studies have shown that newly encoded memories are more resistant to retroactive interference when participants are allowed to sleep after learning the original material, suggesting a sleep-related strengthening of memories. In the present study, we investigated delayed, long-term effects of sleep vs. sleep deprivation (SD) on the first post-training night on memory consolidation and resistance to interference. On day 1, participants learned a list of unrelated word pairs (AB), either in the morning or in the evening, then spent the post-training night in a sleep or sleep deprivation condition, in a within-subject paradigm. On day 4, at the same time of day, they learned a novel list of word pairs (AC) in which 50% of the word pairs stemmed with the same word than in the AB list, resulting in retroactive interference. Participants had then to recall items from the AB list upon presentation of the “A” stem. Recall was marginally improved in the evening, as compared to the morning learning group. Most importantly, retroactive interference effects were found in the sleep evening group only, contrary to the hypothesis that sleep exerts a protective role against intrusion by novel but similar learning. We tentatively suggest that these results can be explained in the framework of the memory reconsolidation theory, stating that exposure to similar information sets back consolidated items in a labile form again sensitive to retroactive interference. In this context, sleep might not protect against interference but would promote an update of existing episodic memories while preventing saturation of the memory network due to the accumulation of dual traces.     

Memory for Expectation-Violating Concepts: The Effects of Agents and Cultural Familiarity

Previous research has shown that ideas which violate our expectations, such as schema-inconsistent concepts, enjoy privileged status in terms of memorability. In our study, memory for concepts that violate cultural (cultural schema-level) expectations (e.g., “illiterate teacher”, “wooden bottle”, or “thorny grass”) versus domain-level (ontological) expectations (e.g., “speaking cat”, “jumping maple”, or “melting teacher”) was examined. Concepts that violate cultural expectations, or counter-schematic, were remembered to a greater extent compared with concepts that violate ontological expectations and with intuitive concepts (e.g., “galloping pony”, “drying orchid”, or “convertible car”), in both immediate recall, and delayed recognition tests. Importantly, concepts related to agents showed a memory advantage over concepts not pertaining to agents, but this was true only for expectation-violating concepts. Our results imply that intuitive, everyday concepts are equally attractive and memorable regardless of the presence or absence of agents. However, concepts that violate our expectations (cultural-schema or domain-level) are more memorable when pertaining to agents (humans and animals) than to non-agents (plants or objects/artifacts). We conclude that due to their evolutionary salience, cultural ideas which combine expectancy violations and the involvement of an agent are especially memorable and thus have an enhanced probability of being successfully propagated.     

“Disorganized in time”: Impact of bottom-up and top-down negative emotion generation on memory formation among healthy and traumatized adolescents

“Travelling in time,” a central feature of episodic memory is severely affected among individuals with Post Traumatic Stress Disorder (PTSD) with two opposite effects: vivid traumatic memories are unorganized in temporality (bottom-up processes), non-traumatic personal memories tend to lack spatio-temporal details and false recognitions occur more frequently that in the general population (top-down processes). To test the effect of these two types of processes (i.e. bottom-up and top-down) on emotional memory, we conducted two studies in healthy and traumatized adolescents, a period of life in which vulnerability to emotion is particularly high. Using negative and neutral images selected from the international affective picture system (IAPS), stimuli were divided into perceptual images (emotion generated by perceptual details) and conceptual images (emotion generated by the general meaning of the material). Both categories of stimuli were then used, along with neutral pictures, in a memory task with two phases (encoding and recognition). In both populations, we reported a differential effect of the emotional material on encoding and recognition. Negative perceptual scenes induced an attentional capture effect during encoding and enhanced the recollective distinctiveness. Conversely, the encoding of conceptual scenes was similar to neutral ones, but the conceptual relatedness induced false memories at retrieval. However, among individuals with PTSD, two subgroups of patients were identified. The first subgroup processed the scenes faster than controls, except for the perceptual scenes, and obtained similar performances to controls in the recognition task. The second subgroup group desmonstrated an attentional deficit in the encoding task with no benefit from the distinctiveness associated with negative perceptual scenes on memory performances. These findings provide a new perspective on how negative emotional information may have opposite influences on memory in normal and traumatized individuals. It also gives clues to understand how intrusive memories and overgeneralization takes place in PTSD.