Wolfgang Klimesch

EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis.

Evidence is presented that EEG oscillations in the alpha and theta band reflect cognitive and memory performance in particular. Good performance is related to two types of EEG phenomena (i) a tonic increase in alpha but a decrease in theta power, and (ii) a large phasic (event-related) decrease in alpha but increase in theta, depending on the type of memory demands. Because alpha frequency shows large interindividual differences which are related to age and memory performance, this double dissociation between alpha vs. theta and tonic vs. phasic changes can be observed only if fixed frequency bands are abandoned. It is suggested to adjust the frequency windows of alpha and theta for each subject by using individual alpha frequency as an anchor point. Based on this procedure, a consistent interpretation of a variety of findings is made possible. As an example, in a similar way as brain volume does, upper alpha power increases (but theta power decreases) from early childhood to adulthood, whereas the opposite holds true for the late part of the lifespan. Alpha power is lowered and theta power enhanced in subjects with a variety of different neurological disorders. Furthermore, after sustained wakefulness and during the transition from waking to sleeping when the ability to respond to external stimuli ceases, upper alpha power decreases, whereas theta increases. Event-related changes indicate that the extent of upper alpha desynchronization is positively correlated with (semantic) long-term memory performance, whereas theta synchronization is positively correlated with the ability to encode new information. The reviewed findings are interpreted on the basis of brain oscillations. It is suggested that the encoding of new information is reflected by theta oscillations in hippocampo-cortical feedback loops, whereas search and retrieval processes in (semantic) long-term memory are reflected by upper alpha oscillations in thalamo-cortical feedback loops.

Memory processes, brain oscillations and EEG synchronization.

This article tries to integrate results in memory research from divergent disciplines such as cognitive psychology, neuroanatomy, and neurophysiology. The integrating link is seen in more recent findings that provide strong arguments for the assumption that oscillations are a basic form of communication between cortical cell assemblies. It is assumed that synchronous oscillations of large cell assemblies--termed type 1 synchronization--reflect a resting state or possibly even a state of functional inhibition. On the other hand, during mental activity, when different neuronal networks may start to oscillate with different frequencies, each network may still oscillate synchronously (this is termed type 2 synchronization), but as a consequence, the large scale type 1 oscillation disappears. It is argued that these different types of synchronization can be observed in the scalp EEG by calculating event-related power changes within comparatively narrow but individually adjusted frequency bands. Experimental findings are discussed which support the hypothesis that short-term (episodic) memory demands lead to a synchronization (increase in band power) in the theta band, whereas long-term (semantic) memory demands lead to a task-specific desynchronization (decrease or suppression of power) in the upper alpha band. Based on these and other findings, a new memory model is proposed that is described on three levels: cognitive, anatomical and neurophysiological. It is suggested that short-term (episodic) memory processes are reflected by oscillations in an anterior limbic system, whereas long-term (semantic) memory processes are reflected by oscillations in a posterior-thalamic system. Oscillations in these frequency bands possibly provide the basis for encoding, accessing, and retrieving cortical codes that are stored in the form of widely distributed but intensely interconnected cell assemblies.

Induced alpha band power changes in the human EEG and attention

Induced alpha power (in a lower, intermediate and upper band) which is deprived from evoked electroencephalograph (EEG) activity was analyzed in an oddball task in which a warning signal (WS) preceded a target or non-target. The lower band, reflecting phasic alertness, desynchronizes only in response to the WS and target. The intermediate band, reflecting expectancy, desynchronizes about 1 s before a target or non-target appears. Upper alpha desynchronizes only after a target is presented and, thus, reflects the performance of the task which was to count the targets. Thus, only slower alpha frequencies reflect attentional demands such as alertness and expectancy.

EEG-alpha rhythms and memory processes

The results of several experiments indicate that alpha frequency varies as a function of memory performance. It was found that in samples of age matched subjects alpha frequency of good memory performers is about 1 Hz-higher than those of bad performers. The difference in alpha frequency between good and bad performers reaches a maximum during the retrieval of information, is much smaller during encoding and is minimal--but still significant--during a resting period. These results suggest that alpha frequency may be a permanent and not only a functional parameter that determines the speed with which information can be retrieved from memory. The calculation of changes in band power indicate further that the upper alpha band is particularly sensitive to semantic memory demands. The lower alpha band, on the other hand, seems to reflect attentional processes. These findings are discussed on the basis of a hypothesis which assumes that EEG frequencies within the alpha band stem at least in part from the thalamus and that the activity of thalamo-cortical networks reflects processes that are related to searching, accessing and retrieving information from (scmantic) long-term memory.

Theta band power in the human scalp EEG and the encoding of new information

TASK-related band power changes in the theta and alpha bands were examined during the encoding of new information in an implicit memory paradigm. The results showed significantly higher theta power during the encoding of those words which could be remembered in the later recall task, compared with words which could not be remembered later. In contrast to the theta band, alpha band power decreased during encoding. However, remembered words, compared with not remembered words did not show significant differences in the the alpha band. The increase in theta power during the successful encoding of new information is discussed with respect to a possible relationship with hippocampal theta, induced in the cortex via hippocampo-cortical feedback loops.

'Paradoxical' alpha synchronization in a memory task

The results of a specially designed memory search paradigm which maximizes episodic short-term memory (STM) and minimizes semantic long-term memory (LTM) demands show that the upper alpha band synchronizes selectively in those conditions and time intervals where episodic STM demands are maximal. This finding of a selective alpha synchronization occurring only in the upper alpha band and during highest task demands is surprising because it is well known that usually alpha desynchronizes during mental activity. Because experiments from our laboratory indicate that desynchronization in the upper alpha band is related to semantic LTM processes, the present finding suggests that a selective synchronization in this frequency band reflects inhibition of semantic LTM. It is assumed that once the capacity limits of STM are reached or exceeded, processing resources are no longer distributed and that potentially interfering, task irrelevant, brain areas or processing systems are inhibited.

Alpha frequency, cognitive load and memory performance.

SummaryEEG-signals were recorded from subjects as they performed a modified version of Schneiders and Shiffrins memory search paradigm. The hypothesis was tested whether individual (centre of gravity) alpha frequency, termed IAF, is related to memory performance and/or attentional demands. The results show that memory performance exerts the strongest effect on IAF. As compared to a resting period, the difference in IAF between age-matched good and bad memory performers reached a maximum when subjects were actually retrieving information from their memory. During retrieval, the IAF of good performers is 1.25 Hz higher than for bad performers. Attentional and task demands also tend to reduce IAF, but- as compared to memory performance - to a much lesser degree. The results of amplitude analyses demonstrate further that during retrieval, alpha desynchronization is more pronounced for bad performers than for good performers. Taken together, the results indicate that a decrease in IAF is always related to a drop in performance.

What does phase information of oscillatory brain activity tell us about cognitive processes

The electroencephalogram (EEG) bears the possibility to investigate oscillatory processes in the human brain. In the animal brain it has been shown that the phase of cortical oscillations is related to the exact timing of neural activity. The potential role of oscillatory phase and phase synchronization for the explanation of cortical information processing has been largely underestimated in the human EEG until now. Here it is argued that EEG phase (synchronization) reflects the exact timing of communication between distant but functionally related neural populations, the exchange of information between global and local neuronal networks, and the sequential temporal activity of neural processes in response to incoming sensory stimuli. Three different kinds of phase synchronization are discussed: (i) phase coupling between brain sites, (ii) phase synchronization across frequencies, and (iii) phase-locking to external events. In this review recent work is presented demonstrating that EEG phase synchronization provides valuable information about the neural correlates of various cognitive processes, and that it leads to a better understanding of how memory and attention processes are interrelated.

Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency.

We applied rapid‐rate repetitive transcranial magnetic stimulation (rTMS) at individual alpha frequency (IAF) to improve cognitive performance by influencing the dynamics of alpha desynchronization. Previous research indicates that a large upper alpha power in a reference interval preceding a task is related to both large suppression of upper alpha power during the task and good performance. Here, we tested the hypothesis that rTMS at individual upper alpha frequency (IAF + 1 Hz) can enhance alpha power in the reference interval, and can thus improve task performance. Repetitive TMS was delivered to the mesial frontal (Fz) and right parietal (P6) cortex, and as sham condition with 90°‐tilted coil (P6 position). The behavioural effect was assessed in a mental rotation task. Further control conditions were rTMS at a lower IAF (IAF − 3 Hz) and at 20 Hz. The results indicate that rTMS at IAF + 1 Hz can enhance task performance and, concomitantly, the extent of task‐related alpha desynchronization. This provides further evidence for the functional relevance of oscillatory neuronal activity in the alpha band for the implementation of cognitive performance.

EEG alpha synchronization and functional coupling during top-down processing in a working memory task

Electroencephalogram (EEG) α (around 10 Hz) is the dominant rhythm in the human brain during conditions of mental inactivity. High amplitudes as observed during rest usually diminish during cognitive effort. During retention of information in working memory, however, power increase of α oscillations can be observed. This α synchronization has been interpreted as cortical idling or active inhibition. The present study provides evidence that during top‐down processing in a working memory task, α power increases at prefrontal but decreases at occipital electrode sites, thereby reaching a state in which α power and frequency become very similar over large distances. Two experimental conditions were compared. In the first, visuospatial information only had to be retained in memory whereas the second condition additionally demanded manipulation of the information. During the second condition, stronger α synchronization at prefrontal sites and larger occipital α suppression was observed as compared to that for pure retention. This effect was accompanied by assimilation of prefrontal and occipital α frequency, stronger functional coupling between prefrontal and occipital brain areas, and α latency shifts from prefrontal cortex to primary visual areas, possibly indicating the control of posterior cortical activation by anterior brain areas. An increase of prefrontal EEG α amplitudes, which is accompanied by a decrease at posterior sites, thus may not be interpreted in terms of idling or “global” inhibition but may enable a tight functional coupling between prefrontal cortical areas, and thereby allows the control of the execution of processes in primary visual brain regions. Hum Brain Mapp, 2005.