Research report
Event-related desynchronization in the alpha band and the processing of semantic information

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Abstract

The hypothesis was tested whether event-related power shifts in the upper alpha band are specifically related to semantic memory processes. In Expt. 1 subjects had to judge whether pairs of sequentially presented words (W1-W2) were semantically congruent. In the following experiments subjects were presented the W1 words of Expt. 1 and were asked to perform a free association task in Expt. 2 and a cued recall task in Expt. 3. It is assumed that semantic memory demands dominate in Expt. 1, whereas working memory demands dominate in Expt. 3 and that Expt. 2 takes an intermediate position with respect to both types of task demands. A significant task-related power change that responds selectively to semantic processing demands was found for the upper alpha band and over the left side of the scalp. The lower alpha band, on the other hand, most likely reflects unspecific processing demands such as attention. A more general interpretation of these findings is that different cognitive processes such as semantic memory, perceptual encoding and attentional processes are reflected by band power changes in different and rather narrow frequency bands over localized regions in the brain.

Introduction

The finding that alpha desynchronizes (becomes suppressed) in response to a variety of different tasks is known since the early days of EEG research (e.g. [2]). It was (and still is) generally believed that visual (or other sensory) task demands, including visual attention (cf. 24, 25), are the primary factors that lead to a suppression of the alpha rhythm. More recent research, however, has revealed a much more complex picture.

A better understanding of the functional meaning of the alpha rhythm was provided by a new method, which Pfurtscheller and his coworkers termed ERD (event-related desynchronization [28]). This method allows to calculate the percentage of event-related power changes for different frequency bands. One important finding obtained with this method is that the degree and topography of desynchronization show large and reliable differences between the lower and upper alpha band. As an example, desynchronization in the lower alpha band is topographically widespread without any clear localization, whereas in the upper alpha band, desynchronization tends to be more localized at those areas which play an important role in processing of a particular type of task. For a variety of motor tasks Pfurtscheller and colleagues (e.g. 23, 29, 30) have demonstrated that desynchronization in the upper alpha band (of about 10–12 Hz) is localized over the respective area of the motor cortex over the left or right side of the scalp. The fact that the two alpha bands show strikingly different results supports the proposal that there is no single alpha rhythm but instead a variety of different alpha frequencies 20, 21.

The method of ERD and the distinction between different alpha bands also proved useful for the analysis of cognitive processes. As an example, a warning signal preceding the presentation of an imperative stimulus causes a strong short-lasting synchronization followed by a desynchronization which most interestingly appears in the lower alpha band only 13, 14, 15. In Expt. 1 of Klimesch et al. [13], subjects were required to read a series of words. The only manipulation was the variation of the time interval between the warning signal and the presentation of a word. For the upper alpha band only the presentation of a word – but not the warning signal – leads to a localized desynchronization at posterior sites 11, 13, 14, 15, 17, 18. In contrast, the lower alpha band responds to the presentation of both, the warning signal and the imperative stimulus. These and similar results (cf. Expt. 2 in Klimesch et al. 13, 15, 17) have led to suggest the hypothesis that the lower alpha band is related to general task demands such as attention (see also Crawford et al. [5]), whereas the upper alpha band is primarily associated with specific task demands such as the visual and/or semantic processing of the imperative stimulus.

This latter aspect of the suggested hypothesis was tested in a more recent experiment which was designed to compare the effects of episodic memory and semantic processing demands [16]. In this experiment we used a design that already proved useful to distinguish semantic from episodic memory processes (see Expt. 4 in Kroll and Klimesch [19]). The experimental design consisted of two parts. Subjects first performed a semantic congruency task in which they had to judge whether or not the sequentially presented words of concept-feature pairs (such as “eagle-claws” or “pea-huge”) are semantically congruent. Then, without prior warning, they were asked to perform an episodic recognition task. This was done in an attempt to prevent subjects from using semantic encoding strategies and thus to increase episodic memory demands. In the episodic task, the same concept-feature pairs were presented together with new distractors (generated by repairing known concept-feature pairs). Now subjects had to judge whether or not a particular concept-feature pair was already presented during the semantic task. From the results found in Kroll and Klimesch [19]we know that the episodic task (showing longer RTs and a larger percentage of incorrect responses) is much more difficult than the semantic task. This latter feature of the design is important for our central prediction which is that upper alpha desynchronizes selectively in response to semantic task demands. When considering the fact that alpha desynchronizes with increasing task difficulty, we would expect the opposite effect, which is a stronger desynchronization during the episodic task. Thus, if task difficulty would be the only factor which is reflected by an event-related decrease in the upper alpha band (reflected by an increase in ERD) we would expect the most pronounced increase in ERD during the presentation of the feature in the episodic task. This, however, is not the case. The results indicate that in spite of the fact that the semantic task is easier than the episodic task, the upper alpha band shows a significantly stronger desynchronization during the processing of the semantic task.

The present experiment is designed to further test the hypothesis whether the upper alpha band is specifically related to the processing of semantic information. The experimental design consists of three different tasks (termed Expt. 1, 2 and 3 in the following) in which semantic processing demands are varied. The same sample of subjects was used in all of the three experiments. In a similar way as in the semantic task of Klimesch et al. [16], in Expt. 1 subjects had to judge whether pairs of sequentially presented words (W1-W2) were semantically congruent. In the following experiments subjects were presented the W1 words of Expt. 1 and were asked to perform a free association task in Expt. 2 and a cued recall task in Expt. 3.

Semantic memory is pure long-term memory [7]. The knowledge about semantic relationships like “an eagle has claws” is known since childhood and represents “pre-experimental knowledge”. On the other hand, “experimental knowledge” is tested in working memory tasks where subjects have to retrieve information that was presented earlier in the experiment [1]. Thus, semantic memory demands vary from high in the semantic congruency task of Expt. 1 to low in the cued recall task of Expt. 3. Conversely, working memory demands are high in Expt. 3 and low in Expt. 1. Expt. 2 takes an intermediate position. In a similar way as in Expt. 1 semantic relationships may be used to give a response. However, in contrast to Expt. 1, subjects may use their working memory either to generate new words or to retrieve the respective W2 words. The term “free association task” is used for Expt. 2 because subjects were instructed explicitly to report any word that comes into their mind.

Given this description of task demands, the following predictions can be tested:

(i) The semantic congruency task of Expt. 1 can be carried out only after the presentation of the second word of a pair. Thus, for the upper alpha band we expect the strongest task-related desynchronization in the poststimulus period following the presentation of the W2 word.

(ii) In contrast to Expt. 1, semantic memory demands are low in Expt. 2 and 3. Thus, as compared to the W2 words of Expt. 1, desynchronization in the upper alpha band will be smaller in Expt. 2 and 3.

(iii) In all of the three experiments, general processing demands, such as attention and effort, will increase from the beginning to the end of a task. For the lower alpha band we, thus, expect a gradual, stepwise increase in desynchronization from the beginning of a trial until a response is given.

Section snippets

Subjects

Subjects were 12 right-handed students (7 males, 5 females) who participated voluntarily in the experiment. Their mean age was 23.7 years with a range of 20–31 years. Handedness was controlled by asking the subjects about the hand they use in different tasks such as handwriting, throwing a ball, etc. A prospective subject was considered right-handed if he/she indicated to use the right hand for all of these different tasks.

Materials

A set of 192 feature and concept words was used as stimuli. Half of the

Behavioral data

In Expt. 1, an average of 5.9% of the responses were incorrect (yes response to an incongruent or no response to a congruent pair). In Expt. 2, in 22.5% of the cases a subject associated the correct concept word, in 31.8% of the cases any concept or feature word that was presented in Expt. 1. An average of 32.8% were new associations. No association or repeated associations were observed in 12.8% of the cases. In Expt. 3, the percentage of correctly remembered concept words was 29.3%

Experiment 1

None of the

Discussion

With respect to the hypothesis that the upper alpha band is specifically related to the processing of semantic information, the most important result is that a significant increase in upper alpha desynchronization was found only during that time interval in which the semantic task actually was carried out (cf. t5 in Fig. 2). Whereas the theta band does not respond to semantic task demands at all, the two lower alpha bands exhibit a stepwise increase in desynchronization that exceeds the level

Acknowledgements

This research was supported by the Austrian “Fonds zur Förderung der wissenschaftlichen Forschung” P-11569. We wish to thank Gernot Florian for his assistance in methodological issues.

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