The medial temporal lobe supports conceptual implicit memory

The medial temporal lobe (MTL) is generally thought to be critical for explicit, but not implicit, memory. Here, we demonstrate that the perirhinal cortex (PRc), within the MTL, plays a role in conceptually-driven implicit memory. Amnesic patients with MTL lesions that converged on the left PRc exhibited deficits on two conceptual implicit tasks (i.e., exemplar generation and semantic decision). A separate functional magnetic resonance imaging (fMRI) study in healthy subjects indicated that PRc activation during encoding of words was predictive of subsequent exemplar generation. Moreover, across subjects, the magnitude of the fMRI and behavioral conceptual priming effects were directly related. Additionally, the PRc region implicated in the fMRI study was the same region of maximal lesion overlap in the patients with impaired conceptual priming. These patient and imaging results converge to suggest that the PRc plays a critical role in conceptual implicit memory, and possibly conceptual processing in general.     

Relational Memory Is Evident in Eye Movement Behavior despite the Use of Subliminal Testing Methods

While it is generally agreed that perception can occur without awareness, there continues to be debate about the type of representational content that is accessible when awareness is minimized or eliminated. Most investigations that have addressed this issue evaluate access to well-learned representations. Far fewer studies have evaluated whether or not associations encountered just once prior to testing might also be accessed and influence behavior. Here, eye movements were used to examine whether or not memory for studied relationships is evident following the presentation of subliminal cues. Participants assigned to experimental or control groups studied scene-face pairs and test trials evaluated implicit and explicit memory for these pairs. Each test trial began with a subliminal scene cue, followed by three visible studied faces. For experimental group participants, one face was the studied associate of the scene (implicit test); for controls none were a match. Subsequently, the display containing a match was presented to both groups, but now it was preceded by a visible scene cue (explicit test). Eye movements were recorded and recognition memory responses were made. Participants in the experimental group looked disproportionately at matching faces on implicit test trials and participants from both groups looked disproportionately at matching faces on explicit test trials, even when that face had not been successfully identified as the associate. Critically, implicit memory-based viewing effects seemed not to depend on residual awareness of subliminal scene cues, as subjective and objective measures indicated that scenes were successfully masked from view. The reported outcomes indicate that memory for studied relationships can be expressed in eye movement behavior without awareness.     

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.     

Implicit associative learning engages the hippocampus and interacts with explicit associative learning

The hippocampus is crucial for conscious, explicit memory, but whether it is also involved in nonconscious, implicit memory is uncertain. We investigated with functional magnetic resonance imaging whether implicit learning engages the hippocampus and interacts with subsequent explicit learning. The presentation of subliminal faces-written profession pairs for implicit learning was followed by the explicit learning of supraliminal pairs composed of the same faces combined with written professions semantically incongruous to those presented subliminally (experiment 1), semantically congruous professions (experiment 2), or identical professions (experiment 3). We found that implicit face-profession learning interacted with explicit face-profession learning in all experiments, impairing the explicit retrieval of the associations. Hippocampal activity increased during the subliminal presentation of face-profession pairs versus face-nonword pairs and correlated with the later impairment of explicit retrieval. These findings suggest that implicit semantic associative learning engages the hippocampus and influences explicit memory.     

The cognitive neuroscience of memory: perspectives from neuroimaging research.

Cognitive neuroscience approaches to memory attempt to elucidate the brain processes and systems that are involved in different forms of memory and learning. This paper examines recent research from brain-damaged patients and neuroimaging studies that bears on the distinction between explicit and implicit forms of memory. Explicit memory refers to conscious recollection of previous experiences, whereas implicit memory refers to the non-conscious effects of past experiences on subsequent performance and behaviour. Converging evidence suggests that an implicit form of memory known as priming is associated with changes in posterior cortical regions that are involved in perceptual processing; some of the same regions may contribute to explicit memory. The hippocampal formation and prefrontal cortex also play important roles in explicit memory. Evidence is presented from recent PET scanning studies that suggests that frontal regions are associated with intentional strategic efforts to retrieve recent experiences, whereas the hippocampal formation is associated with some aspect of the actual recollection of an event.     

Reward-motivated learning: mesolimbic activation precedes memory formation

We examined anticipatory mechanisms of reward-motivated memory formation using event-related FMRI. In a monetary incentive encoding task, cues signaled high- or low-value reward for memorizing an upcoming scene. When tested 24 hr postscan, subjects were significantly more likely to remember scenes that followed cues for high-value rather than low-value reward. A monetary incentive delay task independently localized regions responsive to reward anticipation. In the encoding task, high-reward cues preceding remembered but not forgotten scenes activated the ventral tegmental area, nucleus accumbens, and hippocampus. Across subjects, greater activation in these regions predicted superior memory performance. Within subject, increased correlation between the hippocampus and ventral tegmental area was associated with enhanced long-term memory for the subsequent scene. These findings demonstrate that brain activation preceding stimulus encoding can predict declarative memory formation. The findings are consistent with the hypothesis that reward motivation promotes memory formation via dopamine release in the hippocampus prior to learning.     

Common molecular mechanisms in explicit and implicit memory

Cellular and molecular studies of both implicit and explicit memory suggest that experience-dependent modulation of synaptic strength and structure is a fundamental mechanism by which these memories are encoded and stored within the brain. In this review, we focus on recent advances in our understanding of two types of memory storage: (i) sensitization in Aplysia, a simple form of implicit memory, and (ii) formation of explicit spatial memories in the mouse hippocampus. These two processes share common molecular mechanisms that have been highly conserved through evolution.     

“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.     

Self-Love or Other-Love? Explicit Other-Preference but Implicit Self-Preference

Do humans prefer the self even over their favorite other person? This question has pervaded philosophy and social-behavioral sciences. Psychology’s distinction between explicit and implicit preferences calls for a two-tiered solution. Our evolutionarily-based Dissociative Self-Preference Model offers two hypotheses. Other-preferences prevail at an explicit level, because they convey caring for others, which strengthens interpersonal bonds–a major evolutionary advantage. Self-preferences, however, prevail at an implicit level, because they facilitate self-serving automatic behavior, which favors the self in life-or-die situations–also a major evolutionary advantage. We examined the data of 1,519 participants, who completed an explicit measure and one of five implicit measures of preferences for self versus favorite other. The results were consistent with the Dissociative Self-Preference Model. Explicitly, participants preferred their favorite other over the self. Implicitly, however, they preferred the self over their favorite other (be it their child, romantic partner, or best friend). Results are discussed in relation to evolutionary theorizing on self-deception.     

Do Implicit and Explicit Measures of the Sense of Agency Measure the Same Thing?

The sense of agency (SoA) refers to perceived causality of the self, i.e. the feeling of causing something to happen. The SoA has been probed using a variety of explicit and implicit measures. Explicit measures include rating scales and questionnaires. Implicit measures, which include sensory attenuation and temporal binding, use perceptual differences between self- and externally generated stimuli as measures of the SoA. In the present study, we investigated whether the different measures tap into the same self-attribution processes by determining whether individual differences on implicit and explicit measures of SoA are correlated. Participants performed tasks in which they triggered tones via key presses (operant condition) or passively listened to tones triggered by a computer (observational condition). We replicated previously reported effects of sensory attenuation and temporal binding. Surprisingly the two implicit measures of SoA were not significantly correlated with each other, nor did they correlate with the explicit measures of SoA. Our results suggest that some explicit and implicit measures of the SoA may tap into different processes.     

Neural manifestations of memory with and without awareness

Neurophysiological events responsible for different types of human memory tend to occur concurrently and are therefore difficult to measure independently. To surmount this problem, we produced perceptual priming (indicated by speeded responses) in the absence of conscious remembering. At encoding, faces appeared briefly while subjects' attention was diverted to other stimuli. Faces appeared again in either an implicit or explicit memory test. Neural correlates of priming were identified as brain potentials beginning 270 ms after face onset with more negative amplitudes for repeated than for new faces. Remembered faces, in contrast, activated a different configuration of intracranial sources producing positive potentials maximal at 600-700 ms. We thus disentangled and characterized distinct neural events associated with memory with and without awareness.     

Facial Mimicry and Emotion Consistency: Influences of Memory and Context

This study investigates whether mimicry of facial emotions is a stable response or can instead be modulated and influenced by memory of the context in which the emotion was initially observed, and therefore the meaning of the expression. The study manipulated emotion consistency implicitly, where a face expressing smiles or frowns was irrelevant and to be ignored while participants categorised target scenes. Some face identities always expressed emotions consistent with the scene (e.g., smiling with a positive scene), whilst others were always inconsistent (e.g., frowning with a positive scene). During this implicit learning of face identity and emotion consistency there was evidence for encoding of face-scene emotion consistency, with slower RTs, a reduction in trust, and inhibited facial EMG for faces expressing incompatible emotions. However, in a later task where the faces were subsequently viewed expressing emotions with no additional context, there was no evidence for retrieval of prior emotion consistency, as mimicry of emotion was similar for consistent and inconsistent individuals. We conclude that facial mimicry can be influenced by current emotion context, but there is little evidence of learning, as subsequent mimicry of emotionally consistent and inconsistent faces is similar.     

Memory and anxiety disorders.

Experimental psychopathologists have identified varying patterns in memory bias in people with depressive and anxiety disorders. Individuals suffering from depression tend to exhibit explicit memory deficits for positively-valanced material, and sometimes exhibit biases for retrieving negative self-relevant information as well. Most studies, however, provide scant evidence for implicit memory biases in depression. In contrast to depression, anxiety disorders are rarely associated with enhanced explicit memory for threat-related information (with the exception of panic disorder). Evidence for implicit memory biases for threat in these syndromes is mixed. After providing an overview of findings on memory abnormalities in depressive and anxiety disorders, data from several new studies bearing on posttraumatic stress disorder (PTSD) in Vietnam combat veterans and in women with histories of childhood sexual abuse are presented. Involving directed forgetting, implicit memory and autobiographical cueing paradigms, these experiments point to a pattern of abnormalities linked to PTSD rather than to trauma per se.     

Brain networks of explicit and implicit learning

Are explicit versus implicit learning mechanisms reflected in the brain as distinct neural structures, as previous research indicates, or are they distinguished by brain networks that involve overlapping systems with differential connectivity? In this functional MRI study we examined the neural correlates of explicit and implicit learning of artificial grammar sequences. Using effective connectivity analyses we found that brain networks of different connectivity underlie the two types of learning: while both processes involve activation in a set of cortical and subcortical structures, explicit learners engage a network that uses the insula as a key mediator whereas implicit learners evoke a direct frontal-striatal network. Individual differences in working memory also differentially impact the two types of sequence learning.     

Memory,consciousness and neuroimaging.

Neuroimaging techniques that allow the assessment of memory performance in healthy human volunteers while simultaneously obtaining measurements of brain activity in vivo may offer new information on the neural correlates of particular forms of memory retrieval and their association with consciousness and intention. We consider evidence from studies with positron emission tomography and functional magnetic resonance imaging indicating that priming, a form of implicit retrieval, is associated with decreased activity in various cortical regions. We also consider evidence concerning the question of whether two components of explicit retrieval--intentional or effortful search and successful conscious recollection--are preferentially associated with increased activity in prefrontal and medial temporal regions, respectively. Last, we consider recent efforts to probe the relation between the phenomenological character of remembering and neural activity. In this instance we broaden our scope to include studies employing event-related potentials and consider evidence concerning the neural correlates of qualitatively different forms of memory, including memory that is specifically associated with a sense of self, and the recollection of particular temporal or perceptual features that might contribute to a rich and vivid experience of the past.     

Sleep-Effects on Implicit and Explicit Memory in Repeated Visual Search

In repeated visual search tasks, facilitation of reaction times (RTs) due to repetition of the spatial arrangement of items occurs independently of RT facilitation due to improvements in general task performance. Whereas the latter represents typical procedural learning, the former is a kind of implicit memory that depends on the medial temporal lobe (MTL) memory system and is impaired in patients with amnesia. A third type of memory that develops during visual search is the observers’ explicit knowledge of repeated displays. Here, we used a visual search task to investigate whether procedural memory, implicit contextual cueing, and explicit knowledge of repeated configurations, which all arise independently from the same set of stimuli, are influenced by sleep. Observers participated in two experimental sessions, separated by either a nap or a controlled rest period. In each of the two sessions, they performed a visual search task in combination with an explicit recognition task. We found that (1) across sessions, MTL-independent procedural learning was more pronounced for the nap than rest group. This confirms earlier findings, albeit from different motor and perceptual tasks, showing that procedural memory can benefit from sleep. (2) Likewise, the sleep group compared with the rest group showed enhanced context-dependent configural learning in the second session. This is a novel finding, indicating that the MTL-dependent, implicit memory underlying contextual cueing is also sleep-dependent. (3) By contrast, sleep and wake groups displayed equivalent improvements in explicit recognition memory in the second session. Overall, the current study shows that sleep affects MTL-dependent as well as MTL-independent memory, but it affects different, albeit simultaneously acquired, forms of MTL-dependent memory differentially.     

Falling Out of Time: Enhanced Memory for Scenes Presented at Behaviorally Irrelevant Points in Time in Posttraumatic Stress Disorder (PTSD)

Spontaneous encoding of the visual environment depends on the behavioral relevance of the task performed simultaneously. If participants identify target letters or auditory tones while viewing a series of briefly presented natural and urban scenes, they demonstrate effective scene recognition only when a target, but not a behaviorally irrelevant distractor, appears together with the scene. Here, we show that individuals with posttraumatic stress disorder (PTSD), who witnessed the red sludge disaster in Hungary, show the opposite pattern of performance: enhanced recognition of scenes presented together with distractors and deficient recognition of scenes presented with targets. The recognition of trauma-related and neutral scenes was not different in individuals with PTSD. We found a positive correlation between memory for scenes presented with auditory distractors and re-experiencing symptoms (memory intrusions and flashbacks). These results suggest that abnormal encoding of visual scenes at behaviorally irrelevant events might be associated with intrusive experiences by disrupting the flow of time.     

Exposing racial discrimination: implicit & explicit measures--the My Body, My Story study of 1005 US-born black & white community health center members

Background

To date, research on racial discrimination and health typically has employed explicit self-report measures, despite their potentially being affected by what people are able and willing to say. We accordingly employed an Implicit Association Test (IAT) for racial discrimination, first developed and used in two recent published studies, and measured associations of the explicit and implicit discrimination measures with each other, socioeconomic and psychosocial variables, and smoking.

Methodology/Principal Findings

Among the 504 black and 501 white US-born participants, age 35–64, randomly recruited in 2008–2010 from 4 community health centers in Boston, MA, black participants were over 1.5 times more likely (p<0.05) to be worse off economically (e.g., for poverty and low education) and have higher social desirability scores (43.8 vs. 28.2); their explicit discrimination exposure was also 2.5 to 3.7 times higher (p<0.05) depending on the measure used, with over 60% reporting exposure in 3 or more domains and within the last year. Higher IAT scores for target vs. perpetrator of discrimination occurred for the black versus white participants: for “black person vs. white person”: 0.26 vs. 0.13; and for “me vs. them”: 0.24 vs. 0.19. In both groups, only low non-significant correlations existed between the implicit and explicit discrimination measures; social desirability was significantly associated with the explicit but not implicit measures. Although neither the explicit nor implicit discrimination measures were associated with odds of being a current smoker, the excess risk for black participants (controlling for age and gender) rose in models that also controlled for the racial discrimination and psychosocial variables; additional control for socioeconomic position sharply reduced and rendered the association null.

Conclusions

Implicit and explicit measures of racial discrimination are not equivalent and both warrant use in research on racial discrimination and health, along with data on socioeconomic position and social desirability.     

The functional neuroanatomy of implicit-motion perception or representational momentum

BACKGROUND: When we view static scenes that imply motion - such as an object dropping off a shelf - recognition memory for the position of the object is extrapolated forward. It is as if the object in our mind's eye comes alive and continues on its course. This phenomenon is known as representational momentum and results in a distortion of recognition memory in the implied direction of motion. Representational momentum is modifiable; simply labelling a drawing of a pointed object as 'rocket' will facilitate the effect, whereas the label 'steeple' will impede it. We used functional magnetic resonance imaging (fMRI) to explore the neural substrate for representational momentum. RESULTS: Subjects participated in two experiments. In the first, they were presented with video excerpts of objects in motion (versus the same objects in a resting position). This identified brain areas responsible for motion perception. In the second experiment, they were presented with still photographs of the same target items, only some of which implied motion (representational momentum stimuli). When viewing still photographs of scenes implying motion, activity was revealed in secondary visual cortical regions that overlap with areas responsible for the perception of actual motion. Additional bilateral activity was revealed within a posterior satellite of V5 for the representational momentum stimuli. Activation was also engendered in the anterior cingulate cortex. CONCLUSIONS: Considering the implicit nature of representational momentum and its modifiability, the findings suggest that higher-order semantic information can act on secondary visual cortex to alter perception without explicit awareness.     

Dissociating explicit and procedural-learning based systems of perceptual category learning

A fundamental question is whether people have available one category learning system, or many. Most multiple systems advocates postulate one explicit and one implicit system. Although there is much agreement about the nature of the explicit system, there is less agreement about the nature of the implicit system. In this article, we review a dual systems theory of category learning called competition between verbal and implicit systems (COVIS) developed by Ashby et al. The explicit system dominates the learning of verbalizable, rule-based category structures and is mediated by frontal brain areas such as the anterior cingulate, prefrontal cortex (PFC), and head of the caudate nucleus. The implicit system, which uses procedural learning, dominates the learning of non-verbalizable, information-integration category structures, and is mediated by the tail of the caudate nucleus and a dopamine-mediated reward signal. We review nine studies that test six a priori predictions from COVIS, each of which is supported by the data.