The effect of encoding manipulations on neural correlates of episodic retrieval

The present experiments investigated whether the neural correlates of explicit (conscious) retrieval from episodic memory vary qualitatively according to conditions at encoding, as is predicted by current views of the neural basis of memory retrieval. Event-related potential (ERP) correlates of word stem (e.g. MOT_) cued recall were compared for items studied under different encoding conditions. In Experiment 1, encoding was either 'shallow' or 'deep' whereas in Experiment 2 the presentation modality of the study items was either visual or auditory. In both experiments robust ERP memory effects were observed for stems completed with explicitly retrieved items from each encoding condition. The effects varied in their magnitude, such that they were largest when elicited by the more memorable class of item in each experiment. The scalp distributions of the effects did not differ according to encoding condition, a finding which offers no support for the view that retrieval involves the literal reinstatement of neural activity engaged at the time of encoding. The findings instead point to the existence of a set of retrieval operations that are engaged regardless of the conditions under which retrieved information is encoded.     

Event-related potential evidence that automatic recollection can be voluntarily avoided

Voluntary control processes can be recruited to facilitate recollection in situations where a retrieval cue fails to automatically bring to mind a desired episodic memory. We investigated whether voluntary control processes can also stop recollection of unwanted memories that would otherwise have been automatically recollected. Participants were trained on cue-associate word-pairs, then repeatedly presented with the cue and asked to either recollect or avoid recollecting the associate, while having the event-related potential (ERP) correlate of conscious recollection measured. Halfway through the phase, some cues switched instructions so that participants had to start avoiding recall of associates they had previously repeatedly recalled, and vice versa. ERPs during recollection avoidance showed a significantly reduced positivity in the correlate of conscious recollection, and switching instructions reversed the ERP effect even for items that had been previously repeatedly recalled, suggesting that voluntary control processes can override highly practiced, automatic recollection. Avoiding recollection of particularly prepotent memories was associated with an additional, earlier ERP negativity that was separable from the later voluntary modulation of conscious recollection. The findings have implications for theories of memory retrieval by highlighting the involvement of voluntary attentional processes in controlling conscious recollection.     

Individual differences in executive functioning modulate age effects on the ERP correlates of retrieval success

The present study aimed to investigate whether the level of executive functioning modulated the effects of aging on episodic memory performance and on the electrophysiological correlates of retrieval success (‘old/new effect’). We used a differential approach in which young and older adults were divided into four groups of 14 participants according to their scores on a composite executive index: young-high, young-low, old-high and old-low. ERPs were recorded while participants performed a word-stem cued-recall task. Behavioral results demonstrated that age-related deficits in memory performance were reduced but not eliminated in individuals with a higher executive functioning level. Young participants exhibited ERP old/new effects on frontal and parietal areas. At posterior sites, the effect was entirely left-sided for young-low adults while for young-high participants it was bilateral, maximal at left sites and of greater amplitude. For the old-low group, both frontally-based and parietally-based processes appeared to be affected by the aging process. They also demonstrated a late frontal negative component, which might indicate an unsuccessful additional attempt to cope with retrieval difficulties. In the old-high group, ERP effects on frontal areas were relatively intact while the parietal effect was impaired compared to young adults. However, old-high subjects exhibited earlier, larger and more symmetrical effects than did old-low adults, which was in line with their better memory performance. These findings provide some support for the executive decline hypothesis of cognitive aging by showing that neural correlates of retrieval success in episodic memory are differentially affected by aging according to executive functioning level. They are consistent with the view that a high executive functioning level may help older adults recruit a cerebral pattern which enables them to perform a memory task more efficiently.     

Examining the neural basis of episodic memory: ERP evidence that faces are recollected differently from names

Episodic memory is supported by recollection, the conscious retrieval of contextual information associated with the encoding of a stimulus. Event-Related Potential (ERP) studies of episodic memory have identified a robust neural correlate of recollection—the left parietal old/new effect—that has been widely observed during recognition memory tests. This left parietal old/new effect is believed to provide an index of generic cognitive operations related to recollection; however, it has recently been suggested that the neural correlate of recollection observed when faces are used as retrieval cues has an anterior scalp distribution, raising the possibility that faces are recollected differently from other types of information. To investigate this possibility, we directly compared neural activity associated with remember responses for correctly recognized face and name retrieval cues. Compound face–name stimuli were studied, and at test either a face or a name was presented alone. Participants discriminated studied from unstudied stimuli, and made a remember/familiar decision for stimuli judged ‘old’. Remembering faces was associated with anterior (500–700 ms) and late right frontal old/new effects (700–900 ms), whereas remembering names elicited mid frontal (300–500 ms) and left parietal (500–700 ms) effects. These findings demonstrate that when directly compared, with reference to common episodes, distinct cognitive operations are associated with remembering faces and names. We discuss whether faces can be remembered in the absence of recollection, or whether there may be more than one way of retrieving episodic context.     

The influence of response-time demands on electrophysiological correlates of successful episodic retrieval

Event-related potentials (ERPs) were acquired in two memory retrieval tasks. In Experiment 1 a 2.5 s response-time limit was imposed at test, while in Experiment 2 there was no explicit upper limit. There were no other structural differences between the two experiments. The response-time manipulation did not influence the accuracy of memory judgements, but resulted in qualitative changes in the ERP old/new effects that were elicited in the two tasks. In Experiment 2, the ERP old/new effects from 700 ms post-stimulus onwards comprised a relatively greater positivity for correct judgements to old items in comparison to correct judgements to new items. In keeping with findings in previous studies, this relative positivity was largest at anterior sites over the right hemisphere. In Experiment 1, by contrast, the ERP old/new effects during the same time window were most prominent at right hemisphere central electrode locations, and comprised a relatively greater positivity for correct judgements to new rather than to old test items. In combination, the findings in the two experiments are consistent with the view that the imposition of different response-time demands results in the engagement of neurally and functionally distinct processes during episodic retrieval. The time course of these distinct ERP old/new effects suggests that different post-retrieval monitoring operations were engaged according to the time available to make memory judgements.     

The effect of encoding manipulation on word-stem cued recall: an event-related potential study

The purpose of the present study was to find out whether the neural correlates of explicit retrieval from episodic memory would vary according to conditions at encoding when the words were presented in separate study/test blocks. Event-related potentials (ERPs) were recorded while participants performed a word-stem cued-recall task. Deeply (semantically) studied words were associated with higher levels of recall and faster response times than shallowly (lexically) studied words. Robust ERP old/new effects were observed for each encoding condition. They varied in magnitude, being largest in the semantic condition. As expected, scalp distributions also differed: for deeply studied words, the old/new effect resembled that found in previous ERP studies of word-stem cued-recall tasks (parietal and right frontal effects, between 400-800 and 800-1100 ms post-stimulus), whereas for shallowly studied words, the parietal old/new effect was absent in the latter latency window. These results can be interpreted as reflecting access to different kinds of memory representation depending on the nature of the processing engaged during encoding. Furthermore, differences in the ERPs elicited by new items indicate that subjects adopted different processing strategies in the test blocks following each encoding condition.     

The role of dual-task and task-switch in prospective memory: Behavioural data and neural correlates

Event-based prospective memory (PM) requires remembering the delayed execution of an intended action in response to a pre-specified PM cue while being actively engaged in an ongoing task in which the cue is embedded. To date, experimental paradigms vary as to whether or not they require participants immediately to stop working on the ongoing task whenever they encounter a PM event (cue) and directly switch to the prospective action (task-switch approach). Alternatively, several other paradigms used in the literature encourage participants to continue working on the ongoing task item after the cue, and only then, perform the prospective action (dual-task approach). The present study explores the possible behavioural and electrophysiological effects that both approaches may have on PM performance. Seventeen young adults performed both versions of a standard PM task in a counterbalanced order during which behavioural data and electroencephalogram (EEG) were recorded. Behavioural data showed a decrement in PM performance in the task-switch compared to the dual-task condition. In addition, EEG data revealed differences between the dual-task and task-switch approach in event-related potential (ERP) components associated with response inhibition and with post-retrieval monitoring (i.e. late positive complex). No differences between the two tasks were found with regard to the PM event detection processes (i.e. N300) and the retrieval of the intended action from long-term memory. In sum, findings demonstrate that it does make a difference which task approach is applied and suggest that dual-task and task-switch paradigms may result in different processing and neurophysiological dynamics particularly concerning attentional resources and cognitive control.     

The electrophysiological correlates of recent and remote recollection

Research using event related potentials (ERPs) to explore recognition memory has linked late parietal old/new effects to the recollection of episodic information. In the vast majority of these studies, the retrieval phase immediately follows encoding and consequently, very little is known about the ERP correlates of long term recollection. This is despite the fact that in other areas of the memory literature there is considerable interest in consolidation theories and the way episodic memory changes over time. The present study explored the idea that consolidation and forgetting processes operating over a moderate retention interval can alter the ERP markers of recollection memory. A remember/know test probed memory for stimuli studied either 15 minutes (recent memory) or 1 week (remote memory) prior to the test phase. Results revealed an attenuated late parietal effect for remote compared to recent remember responses, a finding that remained significant even when these recognition judgments were matched for reaction time. Experiments 2a and 2b identified characteristic differences between recent and remote recognition at the behavioural level. The 1 week delay produced an overall decline in recognition confidence and a dramatic loss of episodic detail. These behavioural changes are thought to underlie the ERP effects reported in the first experiment. The results highlight that although the neural basis of memory may exhibit significant changes as the length of the retention interval increases, it is important to consider the extent to which this is a direct effect of time or an indirect effect due to changes in memory quality, such as the amount of detail that can be recollected.     

Comparative electrophysiological and hemodynamic measures of neural activation during memory-retrieval

The spatial and temporal characteristics of the brain processes underlying memory retrieval were studied with both event-related potentials (ERP) and positron emission tomography (PET) techniques. Subjects studied lists of 20 words and then performed episodic (old/new judgment) or semantic (living/nonliving decision) retrieval tasks on multiple four-item test lists, each lasting 10 sec. The PET and ERP measurements at test were assessed in relation to both the task (episodic vs. semantic) and the item (old vs. new or living vs. nonliving). Episodic retrieval was associated with increased blood flow in the right frontal lobe (Brodmann Area 10) and a sustained, slowly developing positive ERP shift recorded from the right frontopolar scalp. Semantic retrieval was associated with increased blood flow in the left frontal (Area 45) and temporal (Area 21) lobes but no clear ERP concomitant. The two retrieval tasks also differed from each other in the ERPs to single items in an early (300-500 ms) time window. Item-related comparisons yielded convergent results mainly if the retrieved information was relevant to the given task (e.g., old/new items during episodic retrieval and living/nonliving items during semantic retrieval). Episodically retrieved old items were associated with increased blood flow in the left medial temporal lobe and a transient increase in the amplitude of the late positive component (500-700 ms) of the ERP. Semantically retrieved living items were associated with increased blood flow in the left frontal cortex and anterior cingulate and a transient late frontal slow wave (700-1,500 ms) in the ERPs. These results indicate that the brain regions engaged in memory retrieval are active in either a sustained or transient manner. They map task-related processes to sustained and item-related processes to transient neural activity. But they also suggest that task-related factors can transiently affect early stages of item processing.     

Further evidence on the effects of vitamin B12 and folate levels on episodic memory functioning: a population-based study of healthy very old adults.

BACKGROUND: The relationship between vitamin status and cognitive functioning has been addressed in several recent studies with inconclusive results. The purpose of this study was to examine separate and combined effects of serum vitamin B12 and folic acid on episodic memory functioning in very old age. METHODS: Four study groups were selected from a population-based sample of healthy very old adults (90-101 years of age): normal B12/normal folic acid, low B12/normal folic acid, normal B12/low folic acid, and low B12/low folic acid. Cutoff levels were set at 180 pmol/L for vitamin B12 and at 13 nmol/L for folic acid. Subjects completed two episodic recall tasks (objects and words) and two episodic recognition tasks (faces and words). RESULTS: Neither vitamin affected recognition or primary memory. Most interesting, although B12 was unrelated to recall performance, subjects with low folic acid levels showed impairment in both word recall and object recall. CONCLUSIONS: These results replicate and extend previous findings that folic acid may be more critical than B12 to memory functioning in late life. The selective effects of folic acid on episodic recall were discussed in terms of encoding and retrieval mechanisms, as well as in relation to brain protein synthesis.     

Examining the development of memory for temporal context and its underlying neural processes using event-related potentials

Time is a critical feature of episodic memory—memory for events from a specific time and place (Tulving, 1972). Previous research indicates that temporal memory (memory for ‘when’) is slower to develop than memory for other details (e.g., ‘what’ and ‘where’), with improvements observed across middle and late childhood. The factors that drive these changes are not yet clear. We used an event-related potential (ERP) recognition memory paradigm to investigate the underlying processes of memory for temporal context in middle to late childhood (7−9-year-olds; 10−12-year-olds) and young adulthood. Behaviorally, we observed age-related improvements in the ability to place events in temporal context. ERP analyses showed old/new effects for children and adults. We also found brain-behavior relations for 1) episodic memory (ERP mean amplitude difference between source hits and correctly identified new trials was correlated to behavioral accuracy), and 2) temporal memory (ERP mean amplitude difference between source hits and source error trials was correlated to accuracy of temporal memory judgments). This work furthers our understanding of the cognitive processes and neural signatures supporting temporal memory development in middle to late childhood, and has implications for episodic memory development more broadly.     

Electrophysiological evidence for the influence of unitization on the processes engaged during episodic retrieval: enhancing familiarity based remembering

Episodic memory depends upon multiple dissociable retrieval processes. Here we investigated the degree to which the processes engaged during successful retrieval are dependent on the properties of the representations that underlie memory for an event. Specifically we examined whether the individual elements of an event can, under some conditions, be unitized, leading to an enhancement of familiarity based responding. Retrieval processes were examined using event-related potential (ERPs) old/new effects, recorded during an associative recognition memory task. The nature of to-be-remembered information was manipulated by using word-pairs as stimuli. At study, participants were asked to remember word-pairs sharing an association (traffic-jam); association+semantic relationship (lemon-orange); or a semantic relationship only (cereal-bread). A behavioural pre-test revealed that association word-pairs were rated as having the most unitized representation. At test, participants were required to recognize if word-pairs were presented in the same pairing as at study, were rearranged from at study, or were entirely new. Behavioural recognition performance was clearly influenced by the nature of the to-be-remembered stimuli, memory being strongest for pairs related purely by association, and weakest for semantic only pairs. ERP old/new effects recorded at test also showed significant differences in the neural correlates of retrieval, depending on stimulus characteristics. The bilateral frontal old/new effect (typically associated with familiarity) was solely elicited by association only pairs. By contrast, the left parietal old/new effect (associated with recollection) was elicited equally by all three conditions. In addition, the late right frontal old/new effect (typically associated with some form of strategic/executive processing) was modulated. This latter effect was initially largest for association only pairs, and subsequently largest for semantic pairs. These findings suggest that the pattern of engagement of familiarity and recollection during successful episodic retrieval is dependent on the properties of the representations that underlie memory for an event.     

The control of memory retrieval: insights from event-related potentials

Effective performance on episodic retrieval tasks requires the ability to flexibly adapt to changing retrieval demands ('retrieval orientations'; [M.D. Rugg, E.L. Wilding, Retrieval processing and episodic memory, Trends Cogn. Sci. 4 (2000) 108-115]). We used event-related potentials (ERP) to examine whether maintaining a specific retrieval orientation and changing flexibly between different retrieval demands are mediated by the same brain systems or whether dissociable aspects of cognitive control are involved. Sixteen participants performed two recognition memory tasks. One required mere old/new decisions for words (general task), whereas the other task required the additional retrieval of each word's study font typeface (specific task). Furthermore, the participants either were asked to perform the same task continuously or to switch between the two tasks after every second test word. ERPs elicited by correctly rejected new (unstudied) words were analyzed. This enabled us to examine the ERP correlates of having adapted and maintained a task instruction as required during continuous blocks and of flexibly changing between retrieval demands during alternating blocks. The ERP analysis revealed more positive-going ERP slow waves for alternating blocks than for continuous blocks over bilateral frontal recording sites. This effect started around 250 ms after the test word and extended for several hundred milliseconds. As it was present for trials requiring a switch to the other task or to stay on the same task between 500 and 750 ms and no differences between the latter two trial types were obtained, it can be assumed that it is more related to general coordination requirements in alternating blocks, rather than to the actual control required to switch the retrieval task set. In addition, contrasting ERPs for the two task types revealed more positive-going ERP slow waves in the specific task than in the general task in the continuous blocks at lateral frontal recording sites between 250 and 700 ms. Together, these findings suggest that there are electrophysiologically dissociable aspects of cognitive control, namely for adapting and maintaining a retrieval orientation and for flexibly changing between varying retrieval demands.     

Memory encoding and retrieval in the aging brain.

Decline in episodic memory, the encoding and retrieval of autobiographical events, is a hallmark of normal cognitive aging. Although the primary causes of this decline remain elusive, event-related brain potential (ERP) studies have contributed to an understanding of age-related episodic memory failure. These data reveal that, although the retrieval-based episodic memory (EM) effect does not differ dramatically between young and older adults, the acquisition-related data suggest a decline in episodic encoding (i.e., semantic elaboration) with increasing age. We conclude that, at the current state of knowledge, encoding deficiencies are more important than retrieval deficits in understanding the causes of episodic memory decline in the older adult.     

Effect of conceptual and lexical errorless versus trial-and-error learning in amnestic mild cognitive impairment

Errorless learning (EL), involving presenting the target information during encoding, is generally considered effective for teaching information to memory-impaired populations. However, evidence suggests that trial-and-error learning (TEL) can benefit healthy older adults’ memory when guesses are conceptually related to the target. To determine whether TEL can benefit persons with mild cognitive impairment (aMCI), 24 participants with aMCI were given cues associated with nine target words. Half the sample received Conceptual cues (e.g., “beverage”) and the other half received Lexical cues (e.g., SC_______). All underwent an EL study phase, in which the target was presented immediately after the cue, and a TEL phase, in which they made guesses from the cue before the target was presented. Cued recall was tested immediately and 24?h later. At immediate but not 24-h delayed recall, EL targets were better remembered than TEL targets in both conditions. Verbal memory performance appeared to explain why certain individuals benefited more from EL relative to TEL, while semantic memory performance appeared to explain why some people benefited more from conceptual than lexical errors. Thus, EL-based memory intervention for aMCI is likely to be more effective than TEL, particularly to the extent that semantic or episodic memory is affected.     

Animal cognition: defining the issues

The assessment of cognitive functions in rodents represents a critical experimental variable in many research fields, ranging from the basic cognitive neurosciences to psychopharmacology and neurotoxicology. The increasing use of animal behavioral tests as 'assays' for the assessment of effects on learning and memory has resulted in a considerable heterogeneity of data, particularly in the field of behavioral and psycho pharmacology. The limited predictive validity of changes in behavioral performance observed in standard animal tests of learning and memory indicates that a renewed effort to scrutinize the validity of these tests is warranted. In humans, levels of processing (effortful vs. automatic) and categories of information (procedural vs. episodic/declarative) are important variables of cognitive operations. The design of tasks that assess the recall of 'episodic' or 'declarative' information appears to represent a particular challenge for research using laboratory rodents. For example, the hypothesis that changes in inspection time for a previously encountered place or object are based on the recall of declarative/episodic information requires substantiation. In order to generalize findings on the effects of neuronal or pharmacological manipulations on learning and memory, obtained from one species and one task, to other species and other tasks, the mediating role of important sets of variables which influence learning and memory (e.g. attentional, affective) needs to be determined. Similar to the view that a neuronal manipulation (e.g. a lesion) represents a theory of the condition modeled (e.g. a degenerative disorder), an animal behavioral task represents a theory of the behavioral/cognitive process of interest. Therefore, the test of hypotheses regarding the validity of procedures used to assess cognitive functions in animals is an inherent part of the research process.     

Cognitive support at episodic encoding and retrieval: similar patterns of utilization in community-based samples of Alzheimer's disease and vascular dementia patients

The hypothesis that Alzheimer's disease (AD) and vascular dementia (VaD) differ in the pattern of episodic memory was examined in this study. Demented patients with AD and VaD and normal old adults were assessed on episodic memory tasks, including free recall and recognition of slowly and rapidly presented unrelated words and free and cued recall of organizable words. Results showed a general deficit in both demented groups across all memory variables, although the AD and VaD patients were indistinguishable across all measures. The normal old showed proficient utilization of more study time, organizability, and category cues. By contrast, the AD and VaD patients were able to benefit from cognitive support only when guidance was provided at both encoding and retrieval. In addition, in the normal old, recall of unrelated words was characterized by a relatively equal contribution from primary and secondary memory, whereas the demented patients relied predominantly on primary memory. The results suggests a similarity between AD and VaD patients with regard to the nature of the episodic memory impairment, despite etiologic differences between the diseases.     

The role of episodic memory in controlled evaluative judgments about attitudes: an event-related potential study

Event-related potentials (ERPs) are unique in their ability to provide information about the timing of activity in the neural networks that perform complex cognitive processes. Given the dearth of extant data from normal controls on the question of whether attitude representations are stored in episodic or semantic memory, the goal here was to study the nature of the memory representations used during conscious attitude evaluations. Thus, we recorded ERPs while participants performed three tasks: attitude evaluations (i.e., agree/disagree), autobiographical cued recall (i.e., You/Not You) and semantic evaluations (i.e., active/inactive). The key finding was that the parietal episodic memory (EM) effect, a well-established correlate of episodic recollection, was elicited by both attitude evaluations and autobiographical retrievals. By contrast, semantic evaluations of the same attitude items elicited less parietal activity, like that elicited by Not You cues, which only access semantic memory. In accord with hemodynamic results, attitude evaluations and autobiographical retrievals also produced overlapping patterns of slow potential (SP) activity from 500 to 900 ms preceding the response over left and right inferior frontal, anterior medial frontal and occipital brain areas. Significantly different patterns of SP activity were elicited in these locations for semantic evaluations and Not You cues. Taken together, the results indicate that attitude representations are stored in episodic memory. Retrieval timing varied as a function of task, with earlier retrievals in both evaluation conditions relative to those in the autobiographical condition. The differential roles and timing of memory retrieval in evaluative judgment and memory retrieval tasks are discussed.     

Cognitive Support at Episodic Encoding and Retrieval: Similar Patterns of Utilization in Community-Based Samples of Alzheimer's Disease and Vascular Dementia Patients

The hypothesis that Alzheimer's disease (AD) and vascular dementia (VaD) differ in the pattern of episodic memory was examined in this study. Demented patients with AD and VaD and normal old adults were assessed on episodic memory tasks, including free recall and recognition of slowly and rapidly presented unrelated words and free and cued recall of organizable words. Results showed a general deficit in both demented groups across all memory variables, although the AD and VaD patients were indistinguishable across all measures. The normal old showed proficient utilization of more study time, organizability, and category cues. By contrast, the AD and VaD patients were able to benefit from cognitive support only when guidance was provided at both encoding and retrieval. In addition, in the normal old, recall of unrelated words was characterized by a relatively equal contribution from primary and secondary memory, whereas the demented patients relied predominantly on primary memory. The results suggests a similarity between AD and VaD patients with regard to the nature of the episodic memory impairment, despite etiologic differences between the diseases.