Effects of normal aging on event-related desynchronization/synchronization during a memory task in humans

Event-related desynchronization (ERD) and event-related synchronization (ERS) of the 1-20Hz EEG frequencies were studied using wavelet transforms in young (n = 10, mean age 22) and elderly subjects (n = 10, mean age 65) performing an auditory Sternberg memory task with words as stimuli. In both age groups, encoding of the four-word memory set elicited ERS in the theta and alpha frequency range. Theta ERS, and ERD in the alpha and beta bands were observed during retrieval. During encoding, the elderly showed greater alpha ERS and smaller theta ERS. During retrieval, smaller alpha ERD and theta ERS was found in the elderly subjects. Also, in the elderly, beta ERD was elicited in the late time window during retrieval. The statistically significant differences between the age groups were more marked during retrieval than during encoding. The results indicate that although the two groups performed equally well behaviorally in the task and the elderly subjects were cognitively intact, normal aging affects oscillatory theta, alpha and beta responses particularly during retrieval from working memory. The ERD/ERS patterns of the elderly resemble those of children found in a recent study, which might suggest that those memory-related brain processes that evolve later in childhood are the first to be affected in older age.     

Electrophysiological correlates of memory processing in early Finnish–Swedish bilinguals

Event-related desynchronization (ERD) and event-related synchronization (ERS) of the 1–30 EEG frequencies were studied in eight early Finnish–Swedish bilinguals during an auditory bilingual Sternberg memory task using Finnish–Swedish cognates as stimuli. Only subtle differences between languages were expected, since cognates have been assumed to have shared conceptual representations in the bilingual memory. Encoding elicited theta and alpha frequency ERS and beta frequency ERD responses in both languages. Retrieval elicited theta ERS and alpha and beta ERD responses. Some statistically significant differences between encoding and retrieval in Finnish versus Swedish emerged: greater theta and alpha ERS responses were observed during encoding in Swedish than during encoding in Finnish. During between-language retrieval, later-appearing theta ERS and alpha ERD responses were elicited as compared to within-language retrieval. These delayed oscillatory responses might reflect the involvement of central executive attentional functions in relation to language switching.     

Brain oscillation and connectivity during a chemistry visual working memory task

Many studies have reported that frontal theta and posterior alpha activities are associated with working memory tasks. However, fewer studies have focused on examining whether or not the frontal alpha or posterior theta can play a role in the working memory task. This study investigates electroencephalography (EEG) dynamics and connectivity among different brain regions' theta and alpha oscillations. The EEG was collected from undergraduate students (n = 64) while they were performing a Sternberg-like working memory task involving chemistry concepts. The results showed that the frontal midline cluster exhibited sustained theta augmentation across the periods of stimulus presentations, maintenance, and probe presentation, suggesting that the frontal midline theta might associate with facilitating the central execute function to maintain information in the working memory. Study of the central parietal and the occipital clusters revealed a sequence of theta augmentation followed by alpha suppression at constant intervals after the onset of stimulus and probe presentations, suggesting that the posterior theta might be associated with sensory processing, theta gating, or stimulus selection. It further suggests that the posterior alpha event-related de-synchronization (ERD) might be linked to direct information flow into and out of the long-term memory (LTM) and precede stimulus recognition. An alternating phasic alpha event-related synchronization (ERS) and ERD following the 1st stimulus and probe presentations were observed at the occipital cluster, in which alpha ERS might be linked to the inhibition of irrelevant information.     

Age-Related Task Sensitivity of Frontal EEG Entropy During Encoding Predicts Retrieval

Age-related declines in memory may be due in part to changes in the complexity of neural activity in the aging brain. Electrophysiological entropy provides an accessible measure of the complexity of ongoing neural activity. In the current study, we calculated the permutation entropy of the electroencephalogram (EEG) during encoding of relevant (to be learned) and irrelevant (to be ignored) stimuli by younger adults, older adults, and older cognitively declined adults. EEG entropy was differentially sensitive to task requirements across groups, with younger and older controls exhibiting greater control of encoding-related activity than older declined participants. Task sensitivity of frontal EEG during encoding predicted later retrieval, in line with previous evidence that cognitive decline is associated with reduced ability to self-initiate encoding-related processes.     

Retrieval monitoring and anosognosia in Alzheimer's disease

This study explored the relationship between episodic memory and anosognosia (a lack of deficit awareness) among patients with mild Alzheimer's disease (AD). Participants studied words and pictures for subsequent memory tests. Healthy older adults made fewer false recognition errors when trying to remember pictures compared with words, suggesting that the perceptual distinctiveness of picture memories enhanced retrieval monitoring (the distinctiveness heuristic). In contrast, although participants with AD could discriminate between studied and nonstudied items, they had difficulty recollecting the specific presentation formats (words or pictures), and they had limited use of the distinctiveness heuristic. Critically, the demands of the memory test modulated the relationship between memory accuracy and anosognosia. Greater anosognosia was associated with impaired memory accuracy when participants with AD tried to remember words but not when they tried to remember pictures. These data further delineate the retrieval monitoring difficulties among individuals with AD and suggest that anosognosia measures are most likely to correlate with memory tests that require the effortful retrieval of nondistinctive information.     

Brain oscillatory 1-30 Hz EEG ERD/ERS responses during the different stages of an auditory memory search task

Event-related desynchronization (ERD) and event-related synchronization (ERS) responses of 1-30 Hz EEG frequencies during the different stages of an auditory Sternberg memory task were examined. The ERD/ERS responses were examined separately for successive memory set items (four) and for the two recognition conditions (YES/NO). The presentation of the memory set elicited ERS responses in the theta and alpha frequencies, and also beta ERD responses. These ERD/ERS responses elicited during encoding were found to evolve with successive memory set item presentation. The ERD/ERS responses elicited during the presentation of the probe dissociated significantly between the two recognition conditions (YES/NO). When the probe was included in the memory set (YES condition), recognition elicited stronger alpha and beta frequency ERD responses as compared to the NO condition. The findings from the current study verify that alpha ERD/ERS responses robustly dissociate between auditory encoding and recognition. The increasing alpha ERS responses with increasing memory set item presentation during encoding may be correlates of the functioning phonological loop, active memory maintenance and/or attention. The alpha ERD responses during recognition are undoubtedly associated with auditory memory search processes and distinguish between previously presented versus not presented verbal material. We propose that alpha ERD/ERS responses reflect explicitly auditory memory processes, discriminating between auditory encoding and recognition. Theta ERS responses may be associated with working memory processes, and possibly more specifically with the functioning of the central executive. Beta ERD/ERS responses may reflect also cognitive and/or memory processing, rather than merely the activity of the motor cortices.     

Brain oscillatory responses to an auditory-verbal working memory task in mild cognitive impairment and Alzheimer's disease.

We report preliminary findings on EEG oscillatory correlates of working memory in mild cognitive impairment (MCI) and Alzheimer's disease (AD). Event-related desynchronization (ERD) and synchronization (ERS) of the 1-20 Hz EEG frequencies were studied using wavelet transforms in elderly controls, MCI patients and mild probable AD patients performing an auditory-verbal Sternberg memory task. Behaviourally, the AD patients made more errors than the controls and the MCI group. Statistically significant differences during the encoding of the memory set were found between the controls and the MCI group, such that the latter group showed ERD in the approximately 10-20 Hz frequencies. The findings may reflect different, compensatory encoding strategies in MCI. During retrieval, the most obvious differences were observed between the controls and the AD group: the ERD in the approximately 7-17 Hz frequencies was absent in the AD group particularly in anterior and left temporal electrode locations. This finding might indicate that AD is associated with deficient lexical-semantic processing during the retrieval phase in working memory tasks. Future studies with larger patient groups are needed to establish the diagnostic value of ERD/ERS patterns in MCI and AD.     

No effect of targeted memory reactivation during slow‐wave sleep on emotional recognition memory

Recent work has suggested that the benefits of sleep for memory consolidation are enhanced for highly salient (versus non‐salient) memories. Using a technique known as targeted memory reactivation, it is possible to selectively strengthen newly learned memories by re‐exposing the sleeping brain to auditory cues. The aim of the current study was to examine whether emotionally salient memories are also more responsive to targeted memory reactivation in slow‐wave sleep than neutral memories. In an initial training phase, participants memorised emotionally negative and neutral pictures, which were each paired with a semantically related sound. Recognition for the pictures was assessed before and after a 90‐min nap opportunity, during which half the sounds were re‐presented during slow‐wave sleep (as assessed via online polysomnographic sleep monitoring). We observed no effect of targeted memory reactivation on the recognition of emotionally negative or neutral memories. Our results highlight the importance of the memory paradigm used to assess targeted memory reactivation, and suggest that the robust and durable nature of recognition memory may make it an insensitive measure of behavioural targeted memory reactivation benefits. To fully assess the impacts of targeted memory reactivation on emotional memory processing in sleep, future studies should adopt experimental paradigms that maximise the salience of emotional stimuli while also providing a sensitive index of memory accuracy.     

Auditory processing indexed by stimulus-induced alpha desynchronization in children.

By means of magnetoencephalography (MEG), we investigated event-related synchronization and desynchronization (ERS/ERD) in auditory cortex activity, recorded from twelve children aged four to six years, while they passively listened to a violin tone and a noise-burst stimulus. Time-frequency analysis using Wavelet Transform was applied to single-trials of source waveforms observed from left and right auditory cortices. Stimulus-induced changes in non-phase-locked activities were evident. ERS in the beta range (13-30 Hz) lasted only for 100 ms after stimulus onset. This was followed by prominent alpha ERD, which showed a clear dissociation between the upper (12 Hz) and lower (8 Hz) alpha range in both left and right auditory cortices for both stimuli. The time courses of the alpha ERD (onset around 300 ms, peak at 500 ms, offset after 1500 ms) were similar to those previously found for older children and adults with auditory memory related tasks. For the violin tone only, the ERD lasted longer in the upper than the lower alpha band. The findings suggest that induced alpha ERD indexes auditory stimulus processing in children without specific cognitive task requirement. The left auditory cortex showed a larger and longer-lasting upper alpha ERD than did the right auditory cortex, likely reflecting hemispheric differences in maturational stages of neural oscillatory mechanisms.     

Frontotemporal Coherence and Executive Functions Contribute to Episodic Memory During Middle Childhood

Contributions of differential behavioral (executive functions) and electrophysiological (frontal-temporal electroencephalogram or EEG coherence) measures to episodic memory performance were examined during middle childhood. Cognitive flexibility and right frontotemporal functional connectivity during encoding (F4/T8), as well as left frontotemporal functional connectivity during retrieval (Fp1/T7), contributed to episodic memory performance in a sample of 9–12-year-olds. These results suggest that executive functions differentially influence episodic memory, as does left and right frontotemporal functional connectivity during different portions of the memory task.     

Cross‐modal distractors modulate oscillatory alpha power: the neural basis of impaired task performance

Unexpected novel sounds capture one's attention, even when irrelevant to the task pursued (e.g., playing video game). This often comes at a cost to the task (e.g., slower responding). The neural basis for this behavioral distraction effect is not well understood and is subject of this study. Our approach was motivated by findings from cuing paradigms suggesting a link between modulations in oscillatory activity and voluntary attention shifts. The current study tested whether oscillatory activity is also modulated by a task‐irrelevant auditory distractor, reflecting a neural signature of an involuntary shift of attention and accounting for the impaired task performance. We reanalyzed magnetoencephalographic data collected via an auditory‐visual distraction paradigm in which a task‐relevant visual stimulus was preceded by a task‐irrelevant sound on each trial. In 87.5% this was a regular sound (Standard); in 12.5% this was a novel sound (Distractor). We compared nonphase locked oscillatory activity in a time window prior to the visual target as a function of the experimental manipulation (Distractor, Standard). We found low power in the pretarget time window for Distractors compared to Standards in the alpha and beta frequency bands. Importantly, individual alpha power correlated with response speed on a trial‐by‐trial basis for the Distractor only. Sources were localized to the occipital cortex, and also to the parietal and supratemporal cortices. These findings support our hypothesis that the distractor‐related alpha power modulation indexes an involuntary shift of attention which accounts for the impaired task performance.     

Isolating the neural mechanisms of age-related changes in human working memory

Working memory (WM), the process by which information is coded into memory, actively maintained and subsequently retrieved, declines with age. To test the hypothesis that age-related changes in prefrontal cortex (PFC) may mediate this WM decline, we used functional MRI to investigate age differences in PFC activity during separate WM task components (encoding, maintenance, retrieval). We found greater PFC activity in younger than older adults only in dorsolateral PFC during memory retrieval. Fast younger subjects showed less dorsolateral PFC activation during retrieval than slow younger subjects, whereas older adults showed the opposite pattern. Thus age-related changes in dorsolateral PFC and not ventrolateral PFC account for WM decline with normal aging.     

Impairment of a cortical event-related desynchronisation during a bimanual load-lifting task in children with autistic disorder

In autism, the abilities of communication are affected, associated with abnormalities of cognitive, sensorial and motor development. In a previous study based on a load-lifting task, we showed impairment of anticipation in children with autism as evidenced by kinematics and eletromyographic recordings [Neurosci. Lett. 348 (2003) 17]. In the present study, we assessed the cortical counterparts of the use of anticipatory postural adjustments in a group of control children and in a group of children with autism. The tasks required maintaining a stable forearm position despite imposed or voluntary lifting of an object placed either on the controlateral forearm or on a support. We investigated the differences between the two groups of children on the Event-Related Desynchronisation (ERD) which precedes movement onset in adults [Electroencephalogr. Clin. Neurophysiol. 46 (1979) 138]. Electroencephalogram (EEG) power evolution of a 6-8-Hz frequency band was averaged before and after imposed or voluntary movement onset. EEG reactivity of control and autistic children did not differ during the imposed unloading condition, but significant differences appeared in the voluntary unloading situations. Before lifting the object, control children showed an ERD above the left motor areas. An ERD also occurred above the right motor areas when the object was placed on their forearm. This indicates that the ERD can also translate the use of anticipatory postural adjustments. By contrast, children with autism did not show an ERD in the two voluntary situations. This suggests a central deficit of anticipation in both postural and motor control in children with autism.     

Alpha‐band desynchronization reflects memory‐specific processes during visual change detection

Recent work investigating physiological mechanisms of working memory (WM) has revealed that modulation of alpha and beta frequency bands within the EEG plays a key role in WM storage. However, the nature of that role is unclear. In the present study, we examined event‐related desynchronization of alpha and beta (α/β‐ERD) elicited by visual tasks with and without a memory component to measure the impact of a WM demand on this electrophysiological marker. We recorded EEG from 60 healthy participants while they completed three variants on a typical change detection task: one in which participants passively viewed the sample array, passive (WM?); one in which participants viewed and attended the sample array in search of a target color but did not memorize the colors, active (WM?); and one in which participants encoded, attended to, and memorized the sample array, active (WM+). Replicating previous findings, we found that active (WM+) elicited robust α/β‐ERD in frontal and posterior electrode clusters and that α‐ERD was significantly associated with WM capacity. By contrast, α/β‐ERD was significantly smaller in the passive (WM?) and active (WM?) tasks, which did not consistently differ from one another. Furthermore, no such relationship was observed between WM capacity and desynchronization in the passive (WM?) or active (WM?) tasks. Taken together, these results suggest that α‐ERD during memory formation reflects a memory‐specific process such as consolidation or maintenance, rather than serving a generalized role in perceptual gating or engagement of attention.     

Intracerebral recording of cortical activity related to self-paced voluntary movements: a Bereitschaftspotential and event-related desynchronization/synchronization. SEEG study

To analyze the distribution of the cortical electrical activity related to self-paced voluntary movements, i.e. the movement-related readiness potentials (Bereitschaftspotential, BP) and the event-related desynchronization (ERD) and synchronization (ERS) of cortical rhythms using intracerebral recordings. EEG was recorded in 14 epilepsy surgery candidates during preoperative video-stereo-EEG monitoring. Subjects performed self-paced hand movements, with their right and left fingers in succession. EEG signals were obtained from a total of 501 contacts using depth electrodes located in primary and nonprimary cortical regions. In accordance with previous studies, BP was found consistently in the primary motor (M1) and somatosensory (S1) cortex, the supplementary motor area (SMA), and in a few recordings also in the cingulate cortex and in the dorsolateral prefrontal and premotor cortex. ERD and ERS of alpha and beta rhythms were also observed in these cortical regions. The distribution of contacts showing ERD or ERS was larger than the distribution of those showing BP. In contrast to BP, ERD and ERS frequently occurred in the lateral and mesial temporal cortex and the inferior parietal lobule. The number of contacts and cortical regions showing ERD and ERS and not BP suggests that the two electrophysiological phenomena are differently involved in the preparation and execution of simple voluntary movements. Substantial differences between BP and ERD in spatial distribution and the widespread topography of ERD/ERS in temporal and higher-order motor regions suggest that oscillatory cortical changes are coupled with cognitive processes supporting movement tasks, such as memory, time interval estimation, and attention.     

Aging magnifies the effects of dopamine transporter and D2 receptor genes on backward serial memory

Aging compromises dopamine transporter (DAT) and receptor mechanisms in the frontostriatal circuitry. In a sample of 1288 younger and older adults, we investigated (i) whether individual differences in genotypes of the DAT gene (i.e., SLC6A3, the DAT variable number of tandem repeat 9/9, 9/10, and 10/10) and in the D2 receptor (DRD2) gene (i.e., the C957T [rs6277] CC and any T) interactively contribute to phenotype variations in episodic memory performance; and (ii) whether these genetic effects are magnified in older adults, because of considerable declines in the dopamine functions. Our results showed that carrying genotypes associated with higher levels of striatal synaptic dopamine (DAT 9/9) and higher density of extrastriatal D2 receptors (C957T CC) were associated with better backward serial recall, an episodic memory task with high encoding and retrieval demands. Critically, the gene-gene interaction effect was reliably stronger in older than in younger adults. In line with the resource modulation hypothesis, our findings suggest that aging-related decline in brain phenotypes (e.g., dopamine functions) could alter the relations between genotypes and behavioral phenotypes (e.g., episodic memory).     

Mild traumatic brain injury: Graph-model characterization of brain networks for episodic memory

Episodic memory is among the cognitive functions that can be affected in the acute phase following mild traumatic brain injury (MTBI). The present study used EEG recordings to evaluate global synchronization and network organization of rhythmic activity during the encoding and recognition phases of an episodic memory task varying in stimulus type (kaleidoscope images, pictures, words, and pseudowords). Synchronization of oscillatory activity was assessed using a linear and nonlinear connectivity estimator and network analyses were performed using algorithms derived from graph theory. Twenty five MTBI patients (tested within days post-injury) and healthy volunteers were closely matched on demographic variables, verbal ability, psychological status variables, as well as on overall task performance. Patients demonstrated sub-optimal network organization, as reflected by changes in graph parameters in the theta and alpha bands during both encoding and recognition. There were no group differences in spectral energy during task performance or on network parameters during a control condition (rest). Evidence of less optimally organized functional networks during memory tasks was more prominent for pictorial than for verbal stimuli.     

Oscillatory EEG correlates of arithmetic strategy use in addition and subtraction

Adults use different strategies in mental arithmetic. For example, they directly retrieve the answer from memory or calculate by means of procedural strategies. Despite growing insight into the hemodynamic and electrophysiological correlates of these strategies, the functional changes in the oscillatory brain dynamics during the use of these strategies remain unknown. In the present high-resolution electroencephalography (EEG) study, we analysed event-related synchronisation (ERS) and desynchronisation (ERD) in the theta and alpha bands while participants solved addition and subtraction problems, which displayed a high probability of retrieval or procedural strategy use. Findings revealed that arithmetic fact retrieval is reflected in left-hemispheric ERS in the theta band, whereas the application of procedural strategies is accompanied by bilateral parietooccipital ERD in the alpha band. The topographical and frequency specificity of the strategy effects provides a start for the development of electrophysiological indices of strategy use in arithmetic. B. De Smedt and R. H. Grabner equally contributed to this study and should be regarded as joint first authors.     

Preservation of crossmodal selective attention in healthy aging

The goal of the present study was to determine if older adults benefited from attention to a specific sensory modality in a voluntary attention task and evidenced changes in voluntary or involuntary attention when compared to younger adults. Suppressing and enhancing effects of voluntary attention were assessed using two cued forced-choice tasks, one that asked participants to localize and one that asked them to categorize visual and auditory targets. Involuntary attention was assessed using the same tasks, but with no attentional cues. The effects of attention were evaluated using traditional comparisons of means and Cox proportional hazards models. All analyses showed that older adults benefited behaviorally from selective attention in both visual and auditory conditions, including robust suppressive effects of attention. Of note, the performance of the older adults was commensurate with that of younger adults in almost all analyses, suggesting that older adults can successfully engage crossmodal attention processes. Thus, age-related increases in distractibility across sensory modalities are likely due to mechanisms other than deficits in attentional processing.     

Exploring memory functions by means of brain electrical topography: A review

Summary A series of experiments is reviewed which explored whether the functional brain state of long-term memory retrieval is correlated with specific changes in slow, DC-like event-related brain potentials. The main results are: (1) Retrieving associations from long-term memory is accompanied by a slow negative shift of 5–10 V which prevails about as long as the retrieval process lasts, i.e., in our experiments, for a period of several seconds. (2) When different types of representations have to be reactivated in memory the slow negative wave shows a clearly distinct topography. The maximum was found in a verbal condition over the left frontal, in a spatial condition over the parietal, and in a color condition over the right occipital to temporal cortex. All these conditions were completely equivalent with respect to the established associative structure, the learning procedure, and the performance criterion. (3) The amplitude of the topographic maximum increases with the number of representations which have to be reactivated. This effect is not due to a non-specific increase of effort but specifically related to the number of activated episodic memory contents which had been experimentally established. In contrast, the reactivation of a priori given semantic association did not become manifest in a specific slow wave effect. These findings are compatible with the idea that memory retrieval implies a reactivation of those cortical cell assemblies in the cortex in which the constituting features of a mnestic entity had originally been processed during perception and learning. The results are also discussed with respect to the possible advantages of EEG and MEG recordings for a cognitive psychophysiology in comparison to other brain imaging techniques as PET or fMRI.This work was supported by grant Ro 529/4 of the German Research Foundation (DFG) assigned to the first author.