A comparison of implicit memory tasks in Korsakoff and alcoholic patients

Korsakoff patients generally perform at a normal level on implicit memory tasks in contrast to explicit memory tasks. While this difference is sometimes explained in terms of different memory systems underlying the tasks, the different roles of perceptual and conceptual/semantic processes in these tasks have also been emphasized: explicit tasks require mainly conceptual/semantic processes and implicit tasks are based principally on perceptual processes. However, it has been suggested recently that conceptual/semantic processes may also be involved in some implicit memory tasks (e.g. a Free Association task). Therefore, the performance of Korsakoff and alcoholic patients is here compared in three implicit memory tasks (Stem Completion, Word Identification and Free Association) and one explicit memory task (Cued Recall), allowing us to disentangle what really matters: the nature of the task (implicit or explicit), or the underlying processes (perceptual or conceptual/semantic). The results show only semantic priming in the Free Association and Cued Recall tasks of the alcoholic patients, suggesting that Korsakoff patients have problems particularly with conceptually-driven processing. The implicit or explicit nature of the memory task is not critical.     

Sparing of perceptual implicit memory despite suppression of the electrophysiological word repetition effect: a study with general anesthetic isoflurane.

OBJECTIVE: Much effort has been devoted to the search for the neurophysiological correlates of implicit memory. A commonly held view is that the early portion (250-500 ms) of the event-related potential (ERP) word repetition effect reflects processes important for perceptual implicit memory whereas the latter portion reflects processes implicated in explicit memory. It is, however, difficult to disentangle with certainty the relative contributions of each form of memory on ERPs since both forms co-exist in normal subjects. To dissociate ERP effect related to implicit and explicit memory, we used isoflurane sedation in normal subjects to suppress explicit remembering while sparing implicit memory. These ERPs were compared with those of non-medicated control subjects. METHODS: Thirteen subjects performed an incidental encoding task for words presented auditorily during the inhalation of a subanesthetic dose of isoflurane. After termination of isoflurane administration, we assessed free recall and recorded ERPs during a syllable completion task (implicit memory) and during a passive listening task (ERP repetition effect). Eleven non-medicated control subjects were tested in a similar manner. RESULTS: The controls showed robust early and late ERP repetition effect. The isoflurane group had implicit memory without free recall and showed no ERP repetition effect. CONCLUSIONS: These findings failed to show an association between any part of the repetition effect and perceptual implicit memory. The results are consistent with the view that processes linked to explicit memory contribute to the ERP repetition effect since there was a marked difference in free recall between the control and isoflurane groups. SIGNIFICANCE: The present study shows that the reversible alterations of memory by general anesthetics can be used to study the neurophysiological correlates of memory processes.     

Sustained activity within the default mode network during an implicit memory task

Recent neuroimaging studies have shown that several brain regions - namely, the posterior cingulate cortex (PCC), ventral medial prefrontal cortex (vmPFC), and the bilateral angular gyrus - are more active during resting states than during cognitive tasks (i.e., default mode network). Although there is evidence showing that the default mode network is associated with unconscious state, it is unclear whether this network is associated with unconscious processing when normal human subjects perform tasks without awareness. We manipulated the level of conscious processing in normal subjects by asking them to perform an implicit and an explicit memory task, and analyzed signal changes in the default mode network for the stimuli versus baseline in both tasks. The functional magnetic resonance imaging (fMRI) analysis showed that the level of activation in regions within this network during the implicit task was not significantly different from that during the baseline, except in the left angular gyrus and the insula. There was strong deactivation for the explicit task when compared with the implicit task in the default mode regions, except in the left angular gyrus and the left middle temporal gyrus. These data suggest that the activity in the default network is sustained and less disrupted when an implicit memory task is performed, but is suspended when explicit retrieval is required. These results provide evidence that the default mode network is associated with unconscious processing when human subjects perform an implicit memory task.     

Hippocampal contribution to implicit configuration memory expressed via eye movements during scene exploration

Although hippocampus unequivocally supports explicit/declarative memory, fewer findings have demonstrated its role in implicit expressions of memory. We tested for hippocampal contributions to an implicit expression of configural/relational memory for complex scenes using eye‐movement tracking during functional magnetic resonance imaging (fMRI) scanning. Participants studied scenes and were later tested using scenes that resembled study scenes in their overall feature configuration but comprised different elements. These configurally similar scenes were used to limit explicit memory, and were intermixed with new scenes that did not resemble studied scenes. Scene configuration memory was expressed through eye movements reflecting exploration overlap (EO), which is the viewing of the same scene locations at both study and test. EO reliably discriminated similar study‐test scene pairs from study‐new scene pairs, was reliably greater for similarity‐based recognition hits than for misses, and correlated with hippocampal fMRI activity. In contrast, subjects could not reliably discriminate similar from new scenes by overt judgments, although ratings of familiarity were slightly higher for similar than new scenes. Hippocampal fMRI correlates of this weak explicit memory were distinct from EO‐related activity. These findings collectively suggest that EO was an implicit expression of scene configuration memory associated with hippocampal activity. Visual exploration can therefore reflect implicit hippocampal‐related memory processing that can be observed in eye‐movement behavior during naturalistic scene viewing. © 2015 Wiley Periodicals, Inc.     

Implicit and explicit memory for spatial information in Alzheimer's disease

There is abundant evidence that memory impairment in dementia in patients with Alzheimer's disease (AD) is related to explicit, conscious forms of memory, whereas implicit, unconscious forms of memory function remain relatively intact or are less severely affected. Only a few studies have been performed on spatial memory function in AD, showing that AD patients' explicit spatial memory is impaired, possibly related to hippocampal dysfunction. However, studies on implicit spatial memory in AD are lacking. The current study set out to investigate implicit and explicit spatial memory in AD patients (n=18) using an ecologically valid computer task, in which participants had to remember the locations of various objects in common rooms. The contribution of implicit and explicit memory functions was estimated by means of the process dissociation procedure. The results show that explicit spatial memory is impaired in AD patients compared with a control group (n=21). However, no group difference was found on implicit spatial function. This indicates that spared implicit memory in AD extends to the spatial domain, while the explicit spatial memory function deteriorates. Clinically, this finding might be relevant, in that an intact implicit memory function might be helpful in overcoming problems in explicit processing.     

The functional neuroanatomy of autobiographical memory: a meta-analysis

Autobiographical memory (AM) entails a complex set of operations, including episodic memory, self-reflection, emotion, visual imagery, attention, executive functions, and semantic processes. The heterogeneous nature of AM poses significant challenges in capturing its behavioral and neuroanatomical correlates. Investigators have recently turned their attention to the functional neuroanatomy of AM. We used the effect-location method of meta-analysis to analyze data from 24 functional imaging studies of AM. The results indicated a core neural network of left-lateralized regions, including the medial and ventrolateral prefrontal, medial and lateral temporal and retrosplenial/posterior cingulate cortices, the temporoparietal junction and the cerebellum. Secondary and tertiary regions, less frequently reported in imaging studies of AM, are also identified. We examined the neural correlates of putative component processes in AM, including, executive functions, self-reflection, episodic remembering and visuospatial processing. We also separately analyzed the effect of select variables on the AM network across individual studies, including memory age, qualitative factors (personal significance, level of detail and vividness), semantic and emotional content, and the effect of reference conditions. We found that memory age effects on medial temporal lobe structures may be modulated by qualitative aspects of memory. Studies using rest as a control task masked process-specific components of the AM neural network. Our findings support a neural distinction between episodic and semantic memory in AM. Finally, emotional events produced a shift in lateralization of the AM network with activation observed in emotion-centered regions and deactivation (or lack of activation) observed in regions associated with cognitive processes.     

Further dissociating the processes involved in recognition memory: an FMRI study

Based on an event-related potential study by Rugg et al. [Dissociation of the neural correlates of implicit and explicit memory. Nature, 392, 595-598, 1998], we attempted to isolate the hemodynamic correlates of recollection, familiarity, and implicit memory within a single verbal recognition memory task using event-related fMRI. Words were randomly cued for either deep or shallow processing, and then intermixed with new words for yes/no recognition. The number of studied words was such that, whereas most were recognized ("hits"), an appreciable number of shallow-studied words were not ("misses"). Comparison of deep hits versus shallow hits at test revealed activations in regions including the left inferior parietal gyrus. Comparison of shallow hits versus shallow misses revealed activations in regions including the bilateral intraparietal sulci, the left posterior middle frontal gyrus, and the left frontopolar cortex. Comparison of hits versus correct rejections revealed a relative deactivation in an anterior left medial-temporal region (most likely the perirhinal cortex). Comparison of shallow misses versus correct rejections did not reveal response decreases in any regions expected on the basis of previous imaging studies of priming. Given these and previous data, we associate the left inferior parietal activation with recollection, the left anterior medial-temporal deactivation with familiarity, and the intraparietal and prefrontal responses with target detection. The absence of differences between shallow misses and correct rejections means that the hemodynamic correlates of implicit memory remain unclear.     

Integrated brain activity in medial temporal and prefrontal areas predicts subsequent memory performance: human declarative memory formation at the system level

After an era in which lesion studies have identified the declarative memory system and its essential anatomical structures, functional imaging and event-related potential studies have begun to delineate the neural underpinnings of declarative memory formation at the system level. By memory formation, we refer to those mnemonic processes present during encoding that transform perceptual representations into enduring memories. Recent studies have revealed that distinct regions in medial temporal and prefrontal areas exhibit more neural activity during successful than unsuccessful memory formation. We attempt to identify the nature of the processes underlying these subsequent memory effects. Reviewed data suggest specific mnemonic operations in the medial temporal lobe that may be integrated with semantic/perceptual operations and subserving operations in the prefrontal cortex. The formation of relational and non-relational memories may be supported by distinct subregions within these two brain regions. While the medial temporal lobe may have a serial organizational structure, with a processing hierarchy, interactions between medial temporal and prefrontal areas seem to occur in a parallel and bi-directional fashion. Interacting with this system, emotionally arousing events enhance neural activity in the amygdala, which in turn may modulate processing in other brain regions responsible for declarative memory formation.     

Selective memory and memory deficits in depressed inpatients

We investigated memory impairment and mood-congruent memory bias in depression, using an explicit memory test and an implicit one. Thirty-six severely depressed inpatients that fulfilled DSM-IV criteria for major depressive disorder and 36 healthy controls matched for sex, age, and educational level participated in the study. Explicit memory was assessed with a free recall task and implicit memory with an anagram solution task. Results showed that depressed and controls differed in explicit memory performance, depending on the amount of cognitive distraction between incidental learning and testing. Implicit memory was not affected. In addition, severely depressed patients showed a mood-congruent memory bias in implicit memory but not in explicit memory. The complex pattern of results is discussed with regard to relevant theories of depression.     

Visual statistical learning deficits in memory-impaired individuals

ABSTRACT

Visual statistical learning (VSL) refers to the learning of environmental regularities. Classically considered an implicit process, one patient with isolated hippocampal damage is severely impaired at VSL tasks, suggesting involvement of explicit memory. Here, we asked whether memory impairment (MI) alone, absent of clear hippocampal pathology, predicted deficits across different VSL tasks. A classic VSL task revealed no learning in MI participants (Exp. 1), while imposing attentional demands (Exp. 2: flicker detection, Exp. 3: gender/location categorization) during familiarization revealed modest residual VSL. MI with nonspecific neural correlates predicted impaired VSL overall, but attentional processes may be harnessed for rehabilitation.     

Neural correlates of prospective memory across the lifespan

OVERVIEW: Behavioural data reveal an inverted U-shaped function in the efficiency of prospective memory from childhood to young adulthood to later adulthood. However, prior research has not directly compared processes contributing to age-related variation in prospective memory across the lifespan, hence it is unclear whether the same factors explain the 'rise and fall' of prospective remembering from childhood to later adulthood. The present study examined this question using a paradigm that allowed us to consider the behavioural and neural correlates of processes associated with the prospective and retrospective components of prospective memory. METHODS: We compared 14 adolescents, 14 young adults, and 14 old adults in a paradigm where the prospective memory task was embedded in a semantic categorization task. RESULTS: The behavioural data revealed an inverted U-shaped function with adolescents and old adults performing poorly relative to young adults. Analyses of the error data revealed that different processes may have contributed to failures of prospective memory in adolescents and older adults. This finding was supported by age differences in ERP-components for cue detection and post-retrieval processes. Additionally, source localization using LORETA revealed different patterns of neural recruitment for adolescents and older adults relative to younger adults. CONCLUSION: Our findings demonstrate that adolescents and older adults show different patterns of behavioural errors and neural recruitment for successful prospective remembering indicating that different processes may contribute to the 'rise and fall' of prospective memory across the lifespan.     

Allocentric memory impaired and egocentric memory intact as assessed by virtual reality in recent-onset schizophrenia

Present evidence suggests that schizophrenia is associated with explicit memory deficits, whereas implicit memory seems to be largely preserved. Virtual reality studies on declarative allocentric memory in schizophrenia are rare, and studies on implicit egocentric memory in schizophrenia are lacking. However, virtual realities have a major advantage for the assessment of spatial navigation and memory formation, as computer-simulated first-person environments can simulate navigation in a large-scale space. Twenty-five subjects with recent-onset schizophrenia were compared with 25 healthy matched control subjects on two virtual reality tasks affording the navigation and learning of a virtual park (allocentric memory) and a virtual maze (egocentric memory). Compared with control subjects, schizophrenia subjects were significantly impaired in learning the virtual park. However, schizophrenia subjects were as able as control subjects to learn the virtual maze. Stronger disorganized symptoms of schizophrenia subjects were significantly related to more errors on the virtual maze. It is concluded that egocentric spatial learning adds to the many other implicit cognitive skills being largely preserved in schizophrenia. Possibly, the more global neural network supporting egocentric spatial learning is less affected than the declarative hippocampal memory system in early stages of schizophrenia and may offer opportunities for compensation in the presence of focal deficits.     

A dissociation between implicit and explicit verbal memory in left temporal lobe epilepsy

PURPOSE: Temporal lobe epilepsy patients are well known to present deficits on explicit verbal memory procedures (e.g., recall, recognition). The integrity of implicit memory procedures in these patients is not established. Previous studies in this area used implicit memory measures contaminated by the effects of explicit memory. METHODS: We examined the integrity of verbal implicit and explicit memory in left temporal lobe epilepsy (LTLE) patients and hypothesized that a clear dissociation in performance would be found with a relative preservation of implicit memory. TLE patients (n = 15) and age- and education-matched healthy normal patients (n = 15) were shown a 40-word study list, followed by a test phase requiring completion of word stems based on the study words or new/unseen words. Experimental conditions involved instructions to provide either the old (study) words or novel/nonlist words when completing the stem. Measures of automaticity and recollection provided uncontaminated indices of implicit and explicit memory, respectively. RESULTS: The data showed a significant difference (p < 0.001) between the patients (Recollection, 0.12; SD, 0.18) and controls (0.50, SD, 0.15) on the measure of explicit memory. In contrast, the patients (Automaticity, 0.51; SD, 0.11) and controls (0.45, SD, 0.18) performed similarly on the implicit memory measure, with patient scores clearly at normative levels based on other Process Dissociation Procedure data. CONCLUSIONS: The data demonstrate the integrity of implicit memory in LTLE patients. Finding a dissociation between the two forms of verbal memory in LTLE patients provides evidence that they rely on different neuroanatomic systems.     

The effects of working memory demands on the neural correlates of prospective memory

Event-related brain potentials (ERPs) were used to examine the reciprocal costs of working and prospective memory loads on the neural correlates of the realization of delayed intentions and the detection of target stimuli. The electrophysiological data revealed several interesting results: (1) distinct modulations of the ERPs were elicited by working memory targets and prospective memory cues, (2) working memory load modulated the amplitude of the N300 elicited by prospective memory cues, (3) prospective memory load was associated with a broadly distributed sustained modulation that began shortly after stimulus onset, and (4) brain-behavior correlations between the neural correlates of prospective memory and working memory varied with the working memory demands of the ongoing activity. These findings appear to indicate that attentional processes associated with the detection of prospective memory cues are sensitive to the working memory demands of the ongoing activity and that different processes may support prospective memory depending on the working memory demands of the ongoing activity.     

Implicit and explicit olfactory memory in people with and without Down syndrome

This study examined differences in implicit and explicit memory performance between people with Down syndrome (DS), their siblings, children matched on mental age, and university undergraduates, using olfactory stimuli. The DS and mental-age matched participants were also compared on two tasks of executive function. The data revealed implicit memory for olfactory stimuli. Further, people with DS performed similarly to each control group on the implicit memory task, but performed significantly poorer than all control groups on the explicit memory task. Impairment to executive functioning was identified as a possible cause of this deficit in explicit memory as people with DS performed more poorly than the mental-age matched controls on both tasks of executive function.     

Primary motor and premotor cortex in implicit sequence learning - evidence for competition between implicit and explicit human motor memory systems

Implicit and explicit memory systems for motor skills compete with each other during and after motor practice. Primary motor cortex (M1) is known to be engaged during implicit motor learning, while dorsal premotor cortex (PMd) is critical for explicit learning. To elucidate the neural substrates underlying the interaction between implicit and explicit memory systems, adults underwent a randomized crossover experiment of anodal transcranial direct current stimulation (AtDCS) applied over M1, PMd or sham stimulation during implicit motor sequence (serial reaction time task, SRTT) practice. We hypothesized that M1‐AtDCS during practice will enhance online performance and offline learning of the implicit motor sequence. In contrast, we also hypothesized that PMd‐AtDCS will attenuate performance and retention of the implicit motor sequence. Implicit sequence performance was assessed at baseline, at the end of acquisition (EoA), and 24 h after practice (retention test, RET). M1‐AtDCS during practice significantly improved practice performance and supported offline stabilization compared with Sham tDCS. Performance change from EoA to RET revealed that PMd‐AtDCS during practice attenuated offline stabilization compared with M1‐AtDCS and sham stimulation. The results support the role of M1 in implementing online performance gains and offline stabilization for implicit motor sequence learning. In contrast, enhancing the activity within explicit motor memory network nodes such as the PMd during practice may be detrimental to offline stabilization of the learned implicit motor sequence. These results support the notion of competition between implicit and explicit motor memory systems and identify underlying neural substrates that are engaged in this competition.     

Neural correlates of word-stem priming

The purpose of this study was to identify the neural correlates of implicit memory in a word-stem completion task. Given that both explicit and implicit retrieval tend to occur in this type of memory task, conventional analyses of old/new event-related potential effects are equivocal. To overcome this problem, depth of processing was manipulated and subjective awareness measured. From 400 ms poststimulus, event-related potentials evoked by stems completed with studied words were more positive than those evoked by stems completed with unstudied items. This difference was maximal at parietooccipital electrode sites. Event-related potentials were not modulated by either depth of processing or awareness. Behavioral and event-related potential data converged to indicate that the old/new effect reflects processes either contributing to, or contingent upon, implicit memory retrieval.     

Intact haptic priming in normal aging and Alzheimer's disease: evidence for dissociable memory systems

This study is the first to report complete priming in Alzheimer's disease (AD) patients and older control subjects for objects presented haptically. To investigate possible dissociations between implicit and explicit objects representations, young adults, Alzheimer's patients, and older controls performed a speeded object naming task followed by a recognition task. Similar haptic priming was exhibited by the three groups, although young adults responded faster than the two older groups. Furthermore, there was no difference in performance between the two healthy groups. On the other hand, younger and older healthy adults did not differ on explicit recognition while, as expected, AD patients were highly impaired. The double dissociation suggests that different memory systems mediate both types of memory tasks. The preservation of intact haptic priming in AD provides strong support to the idea that object implicit memory is mediated by a memory system that is different from the medial-temporal diencephalic system underlying explicit memory, which is impaired early in AD. Recent imaging and behavioral studies suggest that the implicit memory system may depend on extrastriate areas of the occipital cortex although somatosensory cortical mechanisms may also be involved.