Encoding and immediate retrieval tasks in patients with epilepsy: A functional MRI study of verbal and visual memory

Purpose

Medial lobe temporal structures and more specifically the hippocampus play a decisive role in episodic memory. Most of the memory functional magnetic resonance imaging (fMRI) studies evaluate the encoding phase; the retrieval phase being performed outside the MRI. We aimed to determine the ability to reveal greater hippocampal fMRI activations during retrieval phase.

Encoding processes in social anxiety

According to current theories, memory processes play an important role in the maintenance of social fears. However, the empirical evidence regarding memory processes in social anxiety is controversial, and little is known about specific memory processes, such as encoding. The present study employs a release from proactive interference (RPI) technique to explore encoding-related processes in social anxiety. Eighty-four high and low socially anxious college students participated in the RPI task. The main hypothesis was that RPI effects that involve socially threatening words are greater in high than in low socially anxious subjects. Contrary to this hypothesis, however, greater RPI effects were found in low rather than in high socially anxious subjects if a social threat dimension was encoded. This suggests that low socially anxious individuals show more specific encoding strategies of threatening information than high socially anxious individuals.     

Prefrontal contributions to domain-general executive control processes during temporal context retrieval

Neuroimaging studies have reported increased prefrontal cortex (PFC) activity during temporal context retrieval versus recognition memory. However, it remains unclear if these activations reflect PFC contributions to domain-general executive control processes or domain-specific retrieval processes. To gain a better understanding of the functional roles of these various PFC regions during temporal context retrieval we propose it is necessary to examine PFC activity across tasks from different domains, in which parallel manipulations are included targeting specific cognitive processes. In the current fMRI study, we examined domain-general and domain-specific PFC contributions to temporal context retrieval by increasing stimulus (but maintaining response number) and increasing response number (but maintaining stimulus number) across temporal context memory and ordering control tasks, for faces. The control task required subjects to order faces from youngest to oldest. Our behavioral results indicate that the combination of increased stimulus and response numbers significantly increased task difficulty for temporal context retrieval and ordering tasks. Across domains, increasing stimulus number, while maintaining response numbers, caused greater right lateral premotor cortex (BA 6/8) activity; whereas increasing response number, while maintaining stimulus number, caused greater domain-general left DLPFC (BA 9) and VLPFC (BA 44/45) activity. In addition, we found domain-specific right DLPFC (BA 9) activity only during retrieval events. These results highlight the functional heterogeneity of frontal cortex, and suggest its involvement in temporal context retrieval is related to its role in various cognitive control processes.     

Neural correlates of retrieval processing in the prefrontal cortex during recognition and exclusion tasks

Event-related fMRI was employed to contrast the neural activity elicited in prefrontal cortex during recognition memory and exclusion tests. The study phases preceding each memory test were identical, involving the presentation of study items (visually presented words) in one of two study contexts. For the recognition test subjects were required to respond positively to all old items regardless of study context, and to respond negatively to new items. For the exclusion task, positive responses were required to old items presented in one of the study contexts only; negative responses were required both to unstudied items and studied items from the alternative context (non-targets). No prefrontal region demonstrated greater activity for new items in the exclusion task. Thus, there was no evidence that retrieval cues were processed differently according to the specificity of the sought-for information. In several regions, most notably bilateral anterior prefrontal cortex, activity was greater for old than for new items regardless of task. Activity in right dorsolateral prefrontal cortex was also greater for old than for new items; these effects however were larger in the exclusion task. The findings are consistent with previous reports that activity in anterior prefrontal cortex elicited by recognition retrieval cues is sensitive to retrieval success, and extend these findings to the exclusion task. The findings for the right dorsolateral cortex add further weight to the proposal that this region supports post-retrieval monitoring of retrieved information.     

Encoding and retrieval of landmark‐related spatial cues during navigation: An fMRI study

To successfully navigate, humans can use different cues from their surroundings. Learning locations in an environment can be supported by parallel subsystems in the hippocampus and the striatum. We used fMRI to look at differences in the use of object‐related spatial cues while 47 participants actively navigated in an open‐field virtual environment. In each trial, participants navigated toward a target object. During encoding, three positional cues (columns) with directional cues (shadows) were available. During retrieval, the removed target had to be replaced while either two objects without shadows (objects trial) or one object with a shadow (shadow trial) were available. Participants were informed in blocks about which type of retrieval trial was most likely to occur, thereby modulating expectations of having to rely on a single landmark or on a configuration of landmarks. How the spatial learning systems in the hippocampus and caudate nucleus were involved in these landmark‐based encoding and retrieval processes were investigated. Landmark configurations can create a geometry similar to boundaries in an environment. It was found that the hippocampus was involved in encoding when relying on configurations of landmarks, whereas the caudate nucleus was involved in encoding when relying on single landmarks. This might suggest that the observed hippocampal activation for configurations of objects is linked to a spatial representation observed with environmental boundaries. Retrieval based on configurations of landmarks activated regions associated with the spatial updation of object locations for reorientation. When only a single landmark was available during retrieval, regions associated with updating the location of oneself were activated. There was also evidence that good between‐participant performance was predicted by right hippocampal activation. This study therefore sheds light on how the brain deals with changing demands on spatial processing related purely to landmarks. © 2014 Wiley Periodicals, Inc.     

Encoding and retrieval related cerebral activation in continuous verbal recognition

The differential neuronal activation related to encoding of novel and recognition of previously studied items and the effect of retrieval effort on neuronal activation were assessed in a event-related functional magnetic resonance imaging experiment. A verbal continuous recognition task with two repetitions of the target items was used. The interpretation of the results was focused on brain areas that have been previously reported to be involved in explicit memory. Encoding of novel words in comparison with the first repetition was associated with a stronger activation in the left parahippocampal and inferior frontal gyrus. Encoding of novel words compared to the second repetition was related to a greater bifrontal activation. Recognition of studied items was associated with greater activation in the medial and bilateral inferior parietal lobe at first repetition and in the medial and left inferior parietal lobe at second repetition in comparison with encoding of the novel items. Recognition at first repetition compared to recognition at second repetition was associated with greater bilateral frontal activation. The results are discussed in relation to current concepts of spatial differentiation of memory function and findings from event-related potentials studies of continuous recognition.     

Memory retrieval processing: neural indices of processes supporting episodic retrieval

Event-related potentials (ERPs) were acquired during separate test phases of a verbal recognition memory exclusion task in order to contribute to current understanding of the functional significance of differences between ERPs elicited by new (unstudied) test words, which are assumed to index processes engaged in pursuit of task-relevant information. Participants were asked to endorse old words from one study task (targets), and to reject new test words as well as those from a second study task (non-targets). The study task designated as the target category varied across test phases. The left-parietal ERP old/new effect - the electrophysiological signature of recollection - was reliable for targets and for non-targets in all test phases, consistent with the view that participants recollected information about both of these classes of test word. The contrast between the ERPs evoked by new test words separated according to target designation revealed no reliable differences. These findings contrast with those in a recent study in which the same tasks were used, but in which the accuracy of task judgments was markedly higher (Dzulkifli, M.A., & Wilding, E. L. (2005). Electrophysiological indices of strategic episodic retrieval processing. Neuropsychologia, 43, 1152-1162). In that study, there were reliable differences between the ERPs evoked by the two classes of new words, but reliable left-parietal ERP old/new effects for targets only. In combination, the findings suggest that differences between ERPs evoked by new test words can reflect processes that are important for controlling what kinds of information will and will not be recollected.     

Encoding/retrieval dissociation in working memory for human body forms

The present study was conducted to investigate the effect of working memory (WM) load on body processing mechanisms by using event-related potentials (ERPs). It is well known that WM load modulates the P3b (amplitude decreases as WM load increases). Additionally, WM load for faces modulates earlier ERPs like the N170. The present study aimed to investigate the effect of WM load for bodies on the P3b which is associated with WM. Additionally, we explored the effect of WM load on the N170, which is thought to be associated with configural processing, and P1, which has been observed in body as well as in face processing. Effects were analyzed during the encoding and retrieval phases. WM load was modulated by presenting one to four unfamiliar bodies simultaneously for memory encoding. The present study showed that early encoding processes (reflected by the P1 and N170) might not be modulated by WM load, whereas during the retrieval phase, early processes associated with structural encoding (N170) were affected by WM load. A possible explanation of the encoding/retrieval differences might be that subjects used distinct processing strategies in both phases. Parallel encoding of the simultaneously presented bodies might play an important role during the encoding phase where one to four bodies have to be stored, whereas serial matching might be used to compare the probe with the stored pictures during the retrieval phase. Additionally, WM load modulations were observed in later processing steps, which might be associated with stimulus identification and matching processes (reflected by the early P3b) during the encoding but not during the retrieval phase. The current findings further showed for both the encoding and the retrieval phase that the late P3b amplitude decreased as WM load for body images increased indicating that the late P3b is involved in WM processes which do not appear to be category-specific.     

ERP correlates of retrieval orientation: direct versus indirect memory tasks

The neural correlates of the processes involved in cueing memory retrieval were investigated using ERPs to unstudied (new) items in a yes/no recognition test (direct memory task) and a semantic judgement task (indirect memory task). Subjects encoded either pictures or auditory words and were tested on visual words. We replicated previous findings that ERPs to correct rejections of new items in a yes/no recognition test differ according to the study material, with ERPs to words encoded as pictures being more negative (relative to a average mastoid reference) than words encoded auditorily [Hornberger, M., Morcom, A.M., et al., 2004. Neural correlates of retrieval orientation: effects of study-test similarity. J. Cogn. Neurosci. 16 (7), 1196-1210]. This difference was sustained from approximately 450-1,200 ms. An effect of study material on the ERP to new items was found in the indirect memory task but was both earlier onsetting and shorter lived, ca. 250-600 ms. These findings add weight to the concept of 'retrieval orientation' [Rugg, M.D., Wilding, E.L., 2000. Retrieval processing and episodic memory. Trends Cogn. Sci. 4 (3) 108-115] - differential processing of retrieval cues according to the form of the sought-for information - by showing that a putative ERP correlate of retrieval orientation is restricted to direct memory tasks.     

Functional frontoparietal connectivity during encoding and retrieval processes follows HERA model. A high-resolution study

Recent neuroimaging studies of long-term episodic memory have suggested that left prefrontal cortex predominates in encoding condition, whereas right prefrontal cortex predominates in retrieval condition (hemispheric encoding and retrieval asymmetry, HERA model). The present electroencephalographic (EEG) study investigated the functional coupling of fronto-parietal regions during long-term memorization of visuo-spatial contents (i.e. landscapes, interiors of apartments), to test the predictions of the HERA model. Global fronto-parietal coupling was estimated by spectral coherence, whereas the "direction" of the fronto-parietal information flow was estimated by directed transfer function (DTF). The EEG rhythms of interest were theta (4-7 Hz), alpha (8-13 Hz), beta (14-30 Hz), and gamma (30-45 Hz). Statistically significant coherence in line with the HERA model was obtained at the gamma band. Namely, the fronto-parietal gamma coherence prevailed in the left hemisphere during the encoding condition and in the right hemisphere during the retrieval condition. The DTF estimates of the gamma band showed a dominant parietal-to-frontal directional flow in the right hemisphere during the encoding condition and in the left hemisphere during the retrieval condition (i.e. hemisphere-condition combination not involved by the HERA model). In contrast, a balanced bidirectional flow of the fronto-parietal coupling was observed in the left hemisphere during the encoding condition and in the right hemisphere during the retrieval condition (i.e. hemisphere-condition combination involved by the HERA model). In conclusion, the present encoding-retrieval conditions induced maximal fronto-parietal gamma coupling with bidirectional information flow in the hemisphere-condition combination predicted by the HERA model.     

Laboratory-based and autobiographical retrieval tasks differ substantially in their neural substrates

In designing experiments to investigate retrieval of event memory, researchers choose between utilizing laboratory-based methods (in which to-be-remembered materials are presented to participants) and autobiographical approaches (in which the to-be-remembered materials are events from the participant's pre-experimental life). In practice, most laboratory studies have utilized old/new recognition memory, and most autobiographical memory studies have used the Galton-Crovitz word cueing technique [Crovitz, H.F., & Schiffman, H. (1974). Frequency of episodic memories as a function of their age. Bulletin of the Psychonomic Society, 4, 517-518]. What are the implications of these methodological choices for understanding the component processes and underlying neural substrates of memory retrieval? An Activation Likelihood Estimation (ALE) meta-analysis procedure [Turkeltaub, P., Eden, G., Jones, K., & Zeffiro, TA. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation. NeuroImage, 16, 765-780] was used to construct two whole-brain statistical maps: one showing brain regions that are consistently implicated when the task utilized is old/new recognition memory and one showing regions that tend to emerge when autobiographical event memory is queried. A comparison of the two maps shows very few regions of overlap. This basic methodological choice has a profound impact on the conclusions reached regarding human memory retrieval and its neural substrates.     

Role of the frontal lobes in implicit and explicit retrieval tasks

While the role of the frontal lobes in explicit retrieval tasks is well supported, the findings for implicit tasks are less conclusive. We investigated the role of the frontal lobes in perceptual and conceptual implicit priming. Three memory paradigms were given under both implicit and explicit retrieval instructions, using word fragment completion, picture fragment completion and category exemplar generation. Three groups of individuals with frontal lesions were compared to normal controls: Left dorsolateral lesions (n = 5), right dorsolateral lesions (n = 4), and medial lesions (n = 9). Word fragment completion priming was impaired by left dorsolateral lesions, with other priming tests unaffected by any lesion. Explicit performance showed a different pattern, with category exemplar cued recall impaired by left dorsolateral and medial lesions. These findings support the role of the frontal lobes in both implicit and explicit retrieval mechanisms under certain conditions requiring strategy application or lexical retrieval.     

Brain‐derived neurotrophic factor val66met polymorphism and hippocampal activation during episodic encoding and retrieval tasks

Brain‐derived neurotrophic factor (BDNF) is a neurotrophin which has been shown to regulate cell survival and proliferation, as well as synaptic growth and hippocampal long‐term potentiation. A naturally occurring single nucleotide polymorphism in the human BDNF gene (val66met) has been associated with altered intercellular trafficking and regulated secretion of BDNF in met compared to val carriers. Additionally, previous studies have found a relationship between the BDNF val66met genotype and functional activity in the hippocampus during episodic and working memory tasks in healthy young adults. Specifically, studies have found that met carriers exhibit both poorer performance and reduced neural activity within the medial temporal lobe (MTL) when performing episodic memory tasks. However, these studies have not been well replicated and have not considered the role of behavioral differences in the interpretation of neural differences. The current study sought to control for cognitive performance in investigating the role of the BDNF val66met genotype on neural activity associated with episodic memory. Across item and relational memory tests, met carriers exhibited increased MTL activation during both encoding and retrieval stages, compared to noncarriers. The results suggest that met carriers are able to recruit MTL activity to support successful memory processes, and reductions in cognitive performance observed in prior studies are not a ubiquitous effect associated with variants of the BDNF val66met genotype. © 2010 Wiley‐Liss, Inc.     

轻度认知损害患者情节记忆的编码和提取

为了研究轻度认知损害患者情节记忆编码和提取的改变,采用神经心理学方法评定正常老年人和轻度认知损害患者(MCI)情节记忆编码和提取.结果表明:除存在记忆力损害以外,MCI组定向力、语言能力、执行等能力显著低于正常老年组(P《0.01);MCI组患者情节记忆编码正确率显著低于正常老年组(P《0.01),下降约22.81%;MCI组情节记忆提取正确率显著低于正常老年组(P《0.05),下降约6.84%.提示轻度认知损害患者情节记忆编码和提取均存在不同程度的损害,而情节记忆编码的损害更明显.     

轻度认知损害患者情节记忆的编码和提取

为了研究轻度认知损害患者情节记忆编码和提取的改变 ,采用神经心理学方法评定正常老年人和轻度认知损害患者 (MCI)情节记忆编码和提取。结果表明 :除存在记忆力损害以外 ,MCI组定向力、语言能力、执行等能力显著低于正常老年组 (P <0 .0 1) ;MCI组患者情节记忆编码正确率显著低于正常老年组 (P <0 .0 1) ,下降约2 2 .81% ;MCI组情节记忆提取正确率显著低于正常老年组 (P <0 .0 5 ) ,下降约 6 .84 %。提示轻度认知损害患者情节记忆编码和提取均存在不同程度的损害 ,而情节记忆编码的损害更明显。     

Memory deficits and retrieval processes in ALS.

Subtle neuropsychological deficits have been described in patients affected by amyotrophic lateral sclerosis (ALS) without dementia. Overall, selective impairment in memory function has been reported, but the source of memory impairment in ALS has yet to be defined. We performed neuropsychological screening in 20 ALS patients. Semantic encoding and post-encoding cue effects on the retrieval of word lists were investigated in the ALS patients and normal controls. Severity of memory impairment was correlated to cerebral blood perfusion detected by single photon emission computed tomography (SPECT). ALS patients showed moderate impairments in frontal and memory tests. Short-term memory was normal, while serial position retrieval of word lists with normal recency effect but poor primacy effect showed long-term memory deficit. ALS patients performed better in cued encoding than in cued post-encoding recall condition. In the cued post-encoding condition, the primacy effect in word list recall improved significantly in controls, but not in ALS patients, as compared with both the free recall and cued encoding conditions. SPECT hypoperfusion was observed in frontal and temporal areas in ALS patients. ALS patients showed a long-term memory deficit which did not improve in cued post-encoding condition as it does for controls. We hypothesize abnormal retrieval processes related to frontal lobe dysfunction which entails difficulties in generating stable long-memory traces at encoding.     

Gender affects word retrieval of certain categories in semantic fluency tasks.

Recent studies suggest that gender influences phonetically-cued fluency and some semantic memory tasks. In this study we analysed the effect of demographic variables on semantic fluency tasks. The semantic categories considered were: animals, fruits, tools and vehicles. The influence of age and education was common to all the categories considered and seems a general characteristic of the semantic fluency task. Gender had a significant effect only with fruits and tools, but a diverging role: females fared better with fruits and males with tools. We discuss whether the source of the gender effect should be located at the level of the semantic representation of each category or at the level of item recall in the short time (one minute) granted for the task.     

Between-systems memory interference during retrieval

Context memories normally depend on the hippocampus (HPC) but, in the absence of the HPC, other memory systems are capable of acquiring and supporting these memories. This suggests that the HPC can interfere with other systems during memory acquisition. Here we ask whether the HPC can also interfere with the retrieval of a context memory that was independently acquired by a non-HPC system. Specifically, we assess whether the HPC can impair the retrieval of a contextual fear-conditioning memory that was acquired while the HPC was temporarily inactive. Rats were infused with the γ-aminobutyric acid (GABA)(A) receptor agonist muscimol in the dorsal and ventral HPC either before acquisition, retrieval, or prior to both acquisition and retrieval, consistent with the effects of permanent HPC lesions on contextual fear conditioning, if the HPC was inactive at the time of acquisition and retention memory was intact. Thus, non-HPC systems acquired and supported this memory in absence of the HPC. However, if the HPC was inactive during acquisition but active thereafter, rats displayed severe deficits during the retention test. Moreover, when the same rats received a second retention test but with the HPC inactive at this time, the memory was recovered, suggesting that removal of a form of interference allowed the memory to be expressed. Combined, these findings imply that the HPC competes and/or interferes with retrieval of a long-term memory that was established in non-HPC systems.     

Amygdala norepinephrine involved in two separate long-term memory retrieval processes

Noradrenergic manipulation of the rodent amygdala results in time-dependent disruption of long-term memory for a one-trial aversive experience. Findings using both state-dependent and consolidation experimental procedures suggest that the norepinephrine system of the amygdala underlies not only consolidation-like mechanisms. There appear to be specific noradrenergic substrates for two or more memory retrieval processes which may be physiologically similar to either acquisition or later memory development involving aversive information.