Effects of Emotional Context on Memory for Details: The Role of Attention

It was repeatedly demonstrated that a negative emotional context enhances memory for central details while impairing memory for peripheral information. This trade-off effect is assumed to result from attentional processes: a negative context seems to narrow attention to central information at the expense of more peripheral details, thus causing the differential effects in memory. However, this explanation has rarely been tested and previous findings were partly inconclusive. For the present experiment 13 negative and 13 neutral naturalistic, thematically driven picture stories were constructed to test the trade-off effect in an ecologically more valid setting as compared to previous studies. During an incidental encoding phase, eye movements were recorded as an index of overt attention. In a subsequent recognition phase, memory for central and peripheral details occurring in the picture stories was tested. Explicit affective ratings and autonomic responses validated the induction of emotion during encoding. Consistent with the emotional trade-off effect on memory, encoding context differentially affected recognition of central and peripheral details. However, contrary to the common assumption, the emotional trade-off effect on memory was not mediated by attentional processes. By contrast, results suggest that the relevance of attentional processing for later recognition memory depends on the centrality of information and the emotional context but not their interaction. Thus, central information was remembered well even when fixated very briefly whereas memory for peripheral information depended more on overt attention at encoding. Moreover, the influence of overt attention on memory for central and peripheral details seems to be much lower for an arousing as compared to a neutral context.     

“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.     

PRKCA Polymorphism Changes the Neural Basis of Episodic Remembering in Healthy Individuals

Everyday functioning relies on episodic memory, the conscious retrieval of past experiences, but this crucial cognitive ability declines severely with aging and disease. Vulnerability to memory decline varies across individuals however, producing differences in the time course and severity of memory problems that complicate attempts at diagnosis and treatment. Here we identify a key source of variability, by examining gene dependent changes in the neural basis of episodic remembering in healthy adults, targeting seven polymorphisms previously linked to memory. Scalp recorded Event-Related Potentials (ERPs) were measured while participants remembered words, using an item recognition task that requires discrimination between studied and unstudied stimuli. Significant differences were found as a consequence of a Single Nucleotide Polymorphism (SNP) in just one of the tested genes, PRKCA (rs8074995). Participants with the common G/G variant exhibited left parietal old/new effects, which are typically seen in word recognition studies, reflecting recollection-based remembering. During the same stage of memory retrieval participants carrying a rarer A variant exhibited an atypical pattern of brain activity, a topographically dissociable frontally-distributed old/new effect, even though behavioural performance did not differ between groups. Results replicated in a second independent sample of participants. These findings demonstrate that the PRKCA genotype is important in determining how episodic memories are retrieved, opening a new route towards understanding individual differences in memory.     

Rats answer an unexpected question after incidental encoding

A fundamental aspect of episodic memory is that retrieval of information can occur when encoding is incidental and memory assessment is unexpected. These features are difficult to model in animals because behavioral training likely gives rise to well-learned expectations about the sequence of events. Thus, the possibility remains that animals may solve an episodic memory test by using well-learned semantic rules without remembering the episode at memory assessment. Here we show that rats can answer an unexpected question after incidental encoding in a hippocampal-dependent manner, consistent with the use of episodic memory. Rats were initially trained to report about a recent event (food versus no food) and separately searched for food where there was no expectation of being asked about the presence of food. To test episodic memory, we gave rats the opportunity to incidentally encode the presence or absence of food and unexpectedly asked them to report about the recent event. Temporary inactivation of the CA3 region of the hippocampus with bilateral infusions of lidocaine selectively eliminated the ability of rats to answer the unexpected, but not the expected, question. Our studies suggest that rats remember an earlier episode after incidental encoding based upon hippocampal-dependent episodic memory.     

The neural substrates of memory suppression: a FMRI exploration of directed forgetting

The directed forgetting paradigm is frequently used to determine the ability to voluntarily suppress information. However, little is known about brain areas associated with information to forget. The present study used functional magnetic resonance imaging to determine brain activity during the encoding and retrieval phases of an item-method directed forgetting recognition task with neutral verbal material in order to apprehend all processing stages that information to forget and to remember undergoes. We hypothesized that regions supporting few selective processes, namely recollection and familiarity memory processes, working memory, inhibitory and selection processes should be differentially activated during the processing of to-be-remembered and to-be-forgotten items. Successful encoding and retrieval of items to remember engaged the entorhinal cortex, the hippocampus, the anterior medial prefrontal cortex, the left inferior parietal cortex, the posterior cingulate cortex and the precuneus; this set of regions is well known to support deep and associative encoding and retrieval processes in episodic memory. For items to forget, encoding was associated with higher activation in the right middle frontal and posterior parietal cortex, regions known to intervene in attentional control. Items to forget but nevertheless correctly recognized at retrieval yielded activation in the dorsomedial thalamus, associated with familiarity-based memory processes and in the posterior intraparietal sulcus and the anterior cingulate cortex, involved in attentional processes.     

Uncovering camouflage: amygdala activation predicts long-term memory of induced perceptual insight

What brain mechanisms underlie learning of new knowledge from single events? We studied encoding in long-term memory of a unique type of one-shot experience, induced perceptual insight. While undergoing an fMRI brain scan, participants viewed degraded images of real-world pictures where the underlying objects were hard to recognize ("camouflage"), followed by brief exposures to the original images ("solution"), which led to induced insight ("Aha!"). A week later, the participants' memory was tested; a solution image was classified as "remembered" if detailed perceptual knowledge was elicited from the camouflage image alone. During encoding, subsequently remembered images were associated with higher activity in midlevel visual cortex and medial frontal cortex, but most pronouncedly, in the amygdala, whose activity could be used to predict which solutions will remain in long-term memory. Our findings extend the known roles of amygdala in memory to include promotion of long-term memory of the sudden reorganization of internal representations.     

Attention-memory interactions in scene perception

The perception of natural scenes relies on the integration of pre-existing knowledge with the immediate results of attentional processing, and what can be remembered from a scene depends in turn on how that scene is perceived and understood. However, there are conflicting results in the literature as to whether people are more likely to remember those objects that are consistent with the scene or those that are not. Moreover, whether any discrepancy between the likelihood of remembering schema-consistent or schema-inconsistent objects should be attributed to the schematic effects on attention or on memory remains unclear. To address this issue, the current study attempted to directly manipulate attention allocation by requiring participants to look at (i) schema-consistent objects, (ii) schema-inconsistent objects, or (iii) to share attention equally across both. Regardless of the differential allocation of attention or object fixation, schema-consistent objects were better recalled whereas recognition was independent of schema-consistency, but depended on task instruction. These results suggest that attention is important both for remembering low-level object properties, and information whose retrieval is not supported by the currently active schema. Specific knowledge of the scenes being viewed can result in the recall of non-fixated objects, but without such knowledge attention is required to encode sufficient detail for subsequent recognition. Our results demonstrate therefore that attention is not critical for the retrieval of objects that are consistent with a scene's schematic content.     

Retrieval Intention Modulates the Effects of Directed Forgetting Instructions on Recollection

The neurocognitive basis of memory retrieval is often examined by investigating brain potential old/new effects, which are differences in brain activity between successfully remembered repeated stimuli and correctly rejected new stimuli in a recognition test. In this study, we combined analyses of old/new effects for words with an item-method directed-forgetting manipulation in order to isolate differences between the retrieval processes elicited by words that participants were initially instructed to commit to memory and those that participants were initially instructed to forget. We compared old/new effects elicited by to-be-forgotten (TBF) words with those elicited by to-be-remembered (TBR) words in both an explicit-memory test (a recognition test) and an implicit-memory test (a lexical-decision test). Behavioral results showed clear directed forgetting effects in the recognition test, but not in the lexical decision test. Mirroring the behavioral findings, analyses of brain potentials showed evidence of directed forgetting only in the recognition test. In this test, potentials from 450–650 ms (P600 old/new effects) were more positive for TBR relative to TBF words. By contrast, P600 effects evident during the lexical-decision test did not differ in magnitude between TBR and TBF items. When taken in the context of prior studies that have linked similar parietal old/new effects to the recollection of episodic information, these data suggest that directed-forgetting effects manifest primarily in greater episodic retrieval by TBR than TBF items, and that retrieval intention may be important for these directed-forgetting effects to occur.     

Neural basis for successful encoding and retrieval of prospective memory

Prospective memory (PM) refers to memory for future intentions. Difference due to memory (Dm effect) is the difference in neural activity related to stimuli that were subsequently remembered or forgotten. Using event-related potentials (ERPs), the present study investigated the Dm effect for PM using a subsequent task-switching paradigm. The results showed that a Dm effect of ERP P150 was more positive-going for later PM hit trials than for later PM forgotten trials during 100–200 ms. This Dm effect may reflect the process for the production of future intention or the process for attention. Consistent with previously reported Dm effects of other types of memory, we found that the fbN2 (250–280 ms) and late positivity component (400–700 ms) were stronger in later PM hit trials than in forgotten trials. The fbN2 was evoked by Chinese characters. The late positivity component was related to the precise encoding process. In conclusion, because of the early P150, PM encoding appears to be somewhat different from previously identified Dm effects. However, further research is needed. Our findings reveal that Dm effects of PM share similar characteristics with known Dm effects of other types of episodic memory after the very early stage of neural processing.     

Episodic memory and common sense: how far apart?

Research has revealed facts about human memory in general and episodic memory in particular that deviate from both common sense and previously accepted ideas. This paper discusses some of these deviations in light of the proceedings of The Royal Society's Discussion Meeting on episodic memory. Retrieval processes play a more critical role in memory than commonly assumed; people can remember events that never happened; and conscious thoughts about one's personal past can take two distinct forms-'autonoetic' remembering and 'noetic' knowing. The serial-dependent-independent (SPI) model of the relations among episodic, semantic and perceptual memory systems accounts for a number of puzzling phenomena, such as some amnesic patients' preserved recognition memory and their ability to learn new semantic facts, and holds that episodic remembering of perceptual information can occur only by virtue of its mediation through semantic memory. Although common sense endows many animals with the ability to remember their past experiences, as yet there is no evidence that humanlike episodic memory-defined in terms of subjective time, self, and autonoetic awareness-is present in any other species.     

When encoding yields remembering: insights from event-related neuroimaging.

To understand human memory, it is important to determine why some experiences are remembered whereas others are forgotten. Until recently, insights into the neural bases of human memory encoding, the processes by which information is transformed into an enduring memory trace, have primarily been derived from neuropsychological studies of humans with select brain lesions. The advent of functional neuroimaging methods, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), has provided a new opportunity to gain additional understanding of how the brain supports memory formation. Importantly, the recent development of event-related fMRI methods now allows for examination of trial-by-trial differences in neural activity during encoding and of the consequences of these differences for later remembering. In this review, we consider the contributions of PET and fMRI studies to the understanding of memory encoding, placing a particular emphasis on recent event-related fMRI studies of the Dm effect: that is, differences in neural activity during encoding that are related to differences in subsequent memory. We then turn our attention to the rich literature on the Dm effect that has emerged from studies using event-related potentials (ERPs). It is hoped that the integration of findings from ERP studies, which offer higher temporal resolution, with those from event-related fMRI studies, which offer higher spatial resolution, will shed new light on when and why encoding yields subsequent remembering.     

Encoding new episodes and making them stick

How do we encode, store, and retrieve new episodic memories, and what are the computations performed by the hippocampus during this process? One system that has been used to model the brain basis of episodic memory in humans is the study of spatial navigation by path integration in rodents. Here I discuss three exciting new findings focused on encoding or replay of spatial sequences in the rat hippocampus. These findings not only provide important new insight into the computations associated with encoding and consolidation of spatial trajectories, but may also have implications for understanding key aspects of human episodic memory.     

The Importance of Encoding-Related Neural Dynamics in the Prediction of Inter-Individual Differences in Verbal Working Memory Performance

Studies of brain-behaviour interactions in the field of working memory (WM) have associated WM success with activation of a fronto-parietal network during the maintenance stage, and this mainly for visuo-spatial WM. Using an inter-individual differences approach, we demonstrate here the equal importance of neural dynamics during the encoding stage, and this in the context of verbal WM tasks which are characterized by encoding phases of long duration and sustained attentional demands. Participants encoded and maintained 5-word lists, half of them containing an unexpected word intended to disturb WM encoding and associated task-related attention processes. We observed that inter-individual differences in WM performance for lists containing disturbing stimuli were related to activation levels in a region previously associated with task-related attentional processing, the left intraparietal sulcus (IPS), and this during stimulus encoding but not maintenance; functional connectivity strength between the left IPS and lateral prefrontal cortex (PFC) further predicted WM performance. This study highlights the critical role, during WM encoding, of neural substrates involved in task-related attentional processes for predicting inter-individual differences in verbal WM performance, and, more generally, provides support for attention-based models of WM.     

Gradual changes in hippocampal activity support remembering the order of events

The hippocampus is thought to contribute to episodic memory in part by binding stimuli to their spatiotemporal context. The present study examined how hippocampal neuronal populations encode spatial and temporal context as rats performed a task in which they were required to remember the order of trial-unique sequences of odors. The results suggest that a gradual change in the pattern of hippocampal activity served as a temporal context for odor-sampling events and was important for successful subsequent memory of the order of those odors.     

The Effects of a Distracting N-Back Task on Recognition Memory Are Reduced by Negative Emotional Intensity

Memory performance is usually impaired when participants have to encode information while performing a concurrent task. Recent studies using recall tasks have found that emotional items are more resistant to such cognitive depletion effects than non-emotional items. However, when recognition tasks are used, the same effect is more elusive as recent recognition studies have obtained contradictory results. In two experiments, we provide evidence that negative emotional content can reliably reduce the effects of cognitive depletion on recognition memory only if stimuli with high levels of emotional intensity are used. In particular, we found that recognition performance for realistic pictures was impaired by a secondary 3-back working memory task during encoding if stimuli were emotionally neutral or had moderate levels of negative emotionality. In contrast, when negative pictures with high levels of emotional intensity were used, the detrimental effects of the secondary task were significantly attenuated.     

Item, context and relational episodic encoding in humans

Recent functional imaging work supports the view that item and relational memory depend upon distinct encoding operations within the medial temporal lobe. Specifically, emerging findings demonstrate that the level of engagement of perirhinal cortex predicts later memory for individual items, whereas the level of hippocampal processing correlates with later relational memory, or recovery of additional episodic details. Furthermore, recent functional magnetic resonance imaging evidence in humans suggests that medial temporal lobe cortical input structures, the perirhinal and posterior parahippocampal cortices, differentially participate in the encoding of objects and their context, providing domain-specific input to the hippocampus. Taken together, these data help to construct a working model of how distinct medial temporal lobe structures participate in episodic memory formation with domain-general relational binding mechanisms supported by the hippocampus and provide emerging evidence for domain-specificity within the perirhinal and parahippocampal cortices.     

Differential Patterns of Prefrontal MEG Activation during Verbal & Visual Encoding and Retrieval

The spatiotemporal profile of activation of the prefrontal cortex in verbal and non-verbal recognition memory was examined using magnetoencephalography (MEG). Sixteen neurologically healthy right-handed participants were scanned whilst carrying out a modified version of the Doors and People Test of recognition memory. A pattern of significant prefrontal activity was found for non-verbal and verbal encoding and recognition. During the encoding, verbal stimuli activated an area in the left ventromedial prefrontal cortex, and non-verbal stimuli activated an area in the right. A region in the left dorsolateral prefrontal cortex also showed significant activation during the encoding of non-verbal stimuli. Both verbal and non-verbal stimuli significantly activated an area in the right dorsomedial prefrontal cortex and the right anterior prefrontal cortex during successful recognition, however these areas showed temporally distinct activation dependent on material, with non-verbal showing activation earlier than verbal stimuli. Additionally, non-verbal material activated an area in the left anterior prefrontal cortex during recognition. These findings suggest a material-specific laterality in the ventromedial prefrontal cortex during encoding for verbal and non-verbal but also support the HERA model for verbal material. The discovery of two process dependent areas during recognition that showed patterns of temporal activation dependent on material demonstrates the need for the application of more temporally sensitive techniques to the involvement of the prefrontal cortex in recognition memory.     

Episodic-like memory in the rat

A fundamental question in comparative cognition is whether animals remember unique, personal past experiences. It has long been argued that memories for specific events (referred to as episodic memory) are unique to humans. Recently, considerable evidence has accumulated to show that food-storing birds possess critical behavioral elements of episodic memory, referred to as episodic-like memory in acknowledgment of the fact that behavioral criteria do not assess subjective experiences. Here we show that rats have a detailed representation of remembered events and meet behavioral criteria for episodic-like memory. We provided rats with access to locations baited with distinctive (e.g., grape and raspberry) or nondistinctive (regular chow) flavors. Locations with a distinctive flavor replenished after a long but not a short delay, and locations with the nondistinctive flavor never replenished. One distinctive flavor was devalued after encoding its location by prefeeding that flavor (satiation) or by pairing it with lithium chloride (acquired taste aversion), while the other distinctive flavor was not devalued. The rats selectively decreased revisits to the devalued distinctive flavor but not to the nondevalued distinctive flavor. The present studies demonstrate that rats selectively encode the content of episodic-like memories.     

Remembrance of odors past: human olfactory cortex in cross-modal recognition memory

Episodic memory is often imbued with multisensory richness, such that the recall of an event can be endowed with the sights, sounds, and smells of its prior occurrence. While hippocampus and related medial temporal structures are implicated in episodic memory retrieval, the participation of sensory-specific cortex in representing the qualities of an episode is less well established. We combined functional magnetic resonance imaging (fMRI) with a cross-modal paradigm, where objects were presented with odors during memory encoding. We then examined the effect of odor context on neural responses at retrieval when these same objects were presented alone. Primary olfactory (piriform) cortex, as well as anterior hippocampus, was activated during the successful retrieval of old (compared to new) objects. Our findings indicate that sensory features of the original engram are preserved in unimodal olfactory cortex. We suggest that reactivation of memory traces distributed across modality-specific brain areas underpins the sensory qualities of episodic memories.     

The neurobiology of the human memory

Memory can be defined as the ability to acquire, process, store, and retrieve information. Memory is indispensable for learning, adaptation, and survival of every living organism. In humans, the remembering process has acquired great flexibility and complexity, reaching close links with other mental functions, such as thinking and emotions. Changes in synaptic connectivity and interactions among multiple neural networks provide the neurobiological substrates for memory encoding, retention, and consolidation. Memory may be categorized as short-term and long-term memory (according to the storage temporal duration), as implicit and explicit memory (with respect to the consciousness of remembering), as declarative (knowing that [fact]) and procedural (knowing how [skill]) memory, or as sensory (echoic, iconic and haptil), semantic, and episodic memory (according to the various remembering domains). Significant advances have been obtained in understanding memory neurobiology, but much remains to be learned in its cognitive, psychological, and phenomenological aspects.