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

Cognitive Brain Research 6 Ž1997. 83–94

Research report

Event-related desynchronization in the alpha band and the processing of semantic information W. Klimesch ) , M. Doppelmayr, T. Pachinger, H. Russegger Department of Physiological Psychology, UniÕersity of Salzburg, Hellbrunnerstr. 34, A-5020 Salzburg, Austria Accepted 30 April 1997

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 ŽW1-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. q 1997 Elsevier Science B.V. Keywords: Lower alpha; Upper alpha; Desynchronization; Semantic memory; Theta; Episodic memory

1. Introduction The finding that alpha desynchronizes Žbecomes suppressed. in response to a variety of different tasks is known since the early days of EEG research Že.g. w2x.. It was Žand still is. generally believed that visual Žor other sensory. task demands, including visual attention Žcf. w24,25x., 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 Ževent-related desynchronization w28x.. 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, desynchro-

) Corresponding author. Fax: q43 662 8044 5126; E-mail: [email protected]

0926-6410r97r$17.00 q 1997 Elsevier Science B.V. All rights reserved. PII S 0 9 2 6 - 6 4 1 0 Ž 9 7 . 0 0 0 1 8 - 9

nization 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 Že.g. w23,29,30x. have demonstrated that desynchronization in the upper alpha band Žof 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 w20,21x. 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 w13–15x. In Expt. 1 of Klimesch et al. w13x, 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.

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W. Klimesch et al.r CognitiÕe Brain Research 6 (1997) 83–94

For the upper alpha band only the presentation of a word – but not the warning signal – leads to a localized desynchronization at posterior sites w11,13–15,17,18x. In contrast, the lower alpha band responds to the presentation of both, the warning signal and the imperative stimulus. These and similar results Žcf. Expt. 2 in Klimesch et al. w13,15,17x. have led to suggest the hypothesis that the lower alpha band is related to general task demands such as attention Žsee also Crawford et al. w5x., whereas the upper alpha band is primarily associated with specific task demands such as the visual andror 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 w16x. In this experiment we used a design that already proved useful to distinguish semantic from episodic memory processes Žsee Expt. 4 in Kroll and Klimesch w19x.. 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 Žsuch as ‘‘eagleclaws’’ 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 Žgenerated 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 w19x we know that the episodic task Žshowing 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 Žreflected 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 Žtermed 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. w16x, in Expt. 1 subjects had to judge whether pairs of sequentially presented words ŽW1-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 w7x. 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 w1x. 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: Ži. 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. Žii. 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. Žiii. 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.

2. Materials and methods 2.1. Subjects Subjects were 12 right-handed students Ž7 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 consid-

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ered right-handed if hershe indicated to use the right hand for all of these different tasks. 2.2. Materials A set of 192 feature and concept words was used as stimuli. Half of the words belonged to the category ‘‘living’’ Žbirds, fruits, vegetables., the other half to ‘‘non-living’’ Žvehicles, clothes, weapons.. For a detailed description of a similar set of stimuli, including word norms, see Kroll and Klimesch w19x. The words appeared at the center of a computer monitor and were 0.7 cm in height. The length of a word with 10 letters was 5.7 cm. Subjects sat at a distance of 90 cm from the monitor.

Fig. 1. In Expt. 1 subjects had to judge whether pairs of sequentially presented feature words ŽW1. and concept words ŽW2. were semantically congruent. In Expt. 2 subjects were asked to respond with a free association to W1, and in Expt. 3, W1 served as a cue to recall the respective concept word ŽW2.. A warning signal ŽWS. preceded the presentation of W1. Test intervals t1–t5 represent time periods of 500 ms each.

2.3. Design In Expt. 1 subjects had to perform a semantic congruency task on sequentially presented pairs of words W1, W2 by responding ‘‘yes’’ to a congruent and ‘‘no’’ to an incongruent pair Že.g., W1 s claws, W2 s eagle; W1 s blue, W2 s canary.. Subjects were instructed to report as quickly as possible but not before a response signal Žcf. Fig. 1. was presented. The W1 words are also called ‘‘feature words’’, whereas the W2 words represent ‘‘concept words’’. Feature words were paired with concept words ŽW2 words. in a way that half of the pairs were congruent, the other half incongruent. Subjects were informed that word pairs representing a ‘‘feature’’ and a ‘‘concept’’ Že.g., ‘‘claws-eagle’’. will be presented. They were asked to give a positive response if the pair is semantically congruent and a negative response if the pair is incongruent Že.g., ‘‘blue-canary’’.. In Expt. 2 and 3 only half of the W1 words were presented. These were those feature words which in Expt. 1 were paired with congruent concept words. The experimental design is shown in Fig. 1. In Expt. 2 subjects were asked to carry out a free association task. They were instructed to report any word that would come into their minds as quickly as possible but after a response signal was presented. Subjects knew that feature words of Expt. 1 – arranged in a different sequence – will be presented. They were asked to avoid repetitions, i.e., responding with the same association more than once. Finally, in Expt. 3 and without prior warning a cued recall task was performed. Subjects were informed that half of the feature words of Expt. 1 – arranged in a different sequence – will be presented again. But now they were asked to remember and report that concept word that was paired with the respective feature word in the semantic task of Expt. 1. Again, subjects were asked to wait with their response until a response signal appeared on the screen.

The main reason for using only those feature words which were congruent in Expt. 1 was to avoid that the type of response in Expt. 1 Žwhich represents episodic information. interferes or interacts with the type of response in Expt. 2 and 3 in an uncontrolled way. As an example, when trying to remember the corresponding concept word in Expt. 3 subjects could try to remember whether a presented feature word elicited a yes or no response in Expt. 1. A strategy like this would prevent subjects from retrieving the semantic relationship between the feature and concept word. The use of congruent feature words in Expt. 2 and 3 makes it, thus, more likely that a subject’s response is based on task relevant semantic instead of irrelevant episodic information. As indicated by Fig. 1, the EEG is analyzed in time intervals of 500 ms each, preceding and following the presentation of a word. These time intervals are termed t1–t5. Interval t1 represents the prestimulus period. During t2 Žand t4 in Expt. 1. the presented W1 or W2 word is encoded, whereas in t3 Žand t5 in Expt. 1. the primary focus is on the cognitive processing of the respective word. Semantic congruency judgments are easy and, thus, quite fast to perform. As the analysis of reaction times ŽRTs. has shown, the average semantic verification time – as measured from the onset of the W2 word – is less than 1 s Žcf. Expt. 2a in Kroll and Klimesch w19x.. In addition, the results of Expt. 2b in Kroll and Klimesch w19x have shown that Žunder otherwise comparable conditions. lexical verification time Žthe time needed to distinguish a word from a non-word. is 677 ms. Earlier performed experiments w10x have indicated that about 200 ms are needed to carry out the type of motor response that was required in these tasks Ži.e., moving the right finger and pressing the respective response key.. This means that in the first poststimulus interval of 0–500 ms Žt2 or t4 respectively. a word is lexicographically processed, whereas semantic verification or processing takes place primarily during the second poststimulus interval Žt3 or t5 respectively..

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W. Klimesch et al.r CognitiÕe Brain Research 6 (1997) 83–94

2.4. Procedure All of the words were presented for 250 ms on a computer monitor. In all of the experiments, the length of a single trial Žepoch. was 8 s. A brief warning signal Ž3000 Hz, lasting for 250 ms. appeared 1000 ms before a W1 word was presented. The structure of single trials is shown in Fig. 1. In an attempt to avoid artifacts, subjects were asked to maintain fixation by looking at the middle of the screen as soon as an acoustic warning signal appeared. As Fig. 1 illustrates, the response signal Žquestion mark. appeared 1500 ms after presentation onset of a W2 word Žin Expt. 1. or a W1 word Žin Expt. 2 and 3.. This procedure was also used to avoid response artifacts and to obtain poststimulus processing times which are of comparable duration in all of the three conditions. This was done even at the risk of a slight increase in working memory demands at or after t5 or t3 respectively. Subjects responded verbally by saying ‘‘yes’’ or ‘‘no’’ in Expt. 1, by reporting an association in Expt. 2 and by reporting a concept word in Expt. 3. All of the responses were recorded by the experimenter. Each experiment was preceded by a series of four training trials. 2.4.1. Apparatus EEG signals were amplified by a 32-channel biosignal amplifier system Žfrequency response: 0.16–30 Hz., subjected to an anti-aliasing filter bank Žcut-off frequency: 30 Hz, 110 dBroctave. and were then converted to a digital format via a 32-channel ArD converter. Sampling rate was 128 Hz. The data were processed by the B.E.S.T. system of Grossegger and Drbal which is based on a 486 PC. During data acquisition, EEG signals were displayed on-line on a high resolution monitor and stored on disk. 2.4.2. Recordings A set of 22 silver electrodes, attached with a glue paste to the scalp, was used to record EEG signals. Ten electrodes were placed according to the international electrode Ž10–20. placement system, at F3, F4, C3, C4, T3, T4, P3, P4, O1 and O2. From the remaining 12 electrodes, four electrodes were placed over parieto-occipital areas ŽPO3, PO1, PO2, PO4., four electrodes were placed over centroparietal areas ŽCP5, CP1, CP2, CP6., and four electrodes were placed over fronto-central areas ŽFC5, FC1, FC2, FC6.. For the placement of these additional electrodes see, e.g., Herrmann et al. w6x. In addition to the 22 electrodes described above, two mastoid electrodes Žtermed A1 and A2. were attached to the left and right ear. Furthermore, the electrooculogram ŽEOG. was recorded from two pairs of leads in order to register horizontal and vertical eye movements. All data were recorded monopolarly against a common reference placed on the nose. In order to eliminate the effects of the nose reference as well as other types of

artifacts, the EEG recordings were corrected by subtracting the arithmetically averaged mastoid recordings ŽA1 q A2.r2 from all of the monopolar recordings. All of the epochs in each of the three experiments were checked individually for artifacts Žeye blinks, horizontal and vertical eye movements, muscle artifacts, etc.. by visual inspection. Only epochs with a correct yes or no response were used for data analysis. The percentage of epochs that were excluded from data analysis was 5.9% Ži.e., no response to a congruent pair, or yes response to an incongruent pair. in Expt. 1, 12.9% Žmissing association or associations reported more than once. in Expt. 2 and 12.1% Žmissing response or concept word reported more than once. in Expt. 3. 2.4.3. The calculation of eÕent-related changes in band power The data for each epoch and each of the 22 channels were digitally band-pass filtered, squared Žin order to obtain simple power estimates. and averaged separately for each experimental condition and for each subject. Based on these data, event-related changes in band power were calculated in using a procedure which was originally proposed by Pfurtscheller and Aranibar w28x who coined the term event-related desynchronization or ERD. ERD is defined as the percentage of decrease or increase in band power during a test interval as compared to a reference interval: ERD % s wŽband power, reference interval. y Žband power, test interval.xrŽband power, reference interval.4 = 100. For a detailed description see e.g. w31x. Note that positive ERD values indicate a state of desynchronization or power suppression. Negative ERD values, on the other hand, reflect a state of synchronization or increase in band power. In the present study, an interval of 1000 ms Žbeginning 2500 ms before and ending 1500 ms before the presentation of the feature word. was used as reference interval Žcf. Fig. 1.. The test intervals consist of time intervals of 500 ms preceding and following the presentation of a word Žcf. the time intervals t1–t5 in Fig. 1.. After rejecting artifacts, an average of 147, 56 and 63 epochs remained for Expt. 1, 2 and 3 respectively. 2.4.4. The indiÕidual determination of frequency bands The frequency windows for the theta and alpha bands were determined individually for each subject i by using mean peak frequency fŽi. of the dominant EEG frequency in the alpha band for all recording sites as an anchor point. Mean peak frequency fŽi. was calculated over the entire epoch of 8 s. In using fŽi. as individual anchor point, four different frequency bands with a bandwidth of 2 Hz each were defined: ŽfŽi.-6. to ŽfŽi.-4.; ŽfŽi.-4. to ŽfŽi.-2.; ŽfŽi.-2. to fŽi.; fŽi. to ŽfŽi. q 2.. The ERD was calculated within these individually determined frequency bands which are termed theta, lower-1 alpha, lower-2 alpha, and upper alpha. The averaged mean frequency fŽi. was 10.0 Hz.

W. Klimesch et al.r CognitiÕe Brain Research 6 (1997) 83–94

Thus, averaged over the entire sample of 12 subjects, the following cut-off points were obtained: 4–6 Hz, 6–8 Hz, 8–10 Hz, 10–12 Hz. With frequency bands of 2 Hz, epochs down to a length of 0.5 s can still be analyzed. However, the effects of spectral leakage Ži.e., the influence of neighboring frequency bands. becomes the more severe, the shorter the epoch length is. One way to compensate for this effect is to use a large number of epochs over which power estimates are averaged. By averaging, the distorting effects of neighboring frequency bands decrease and the accuracy of power estimates increases. This is for the same reason why the accuracy of any estimate increases with increasing sample size. Because only the averaged data Žof at least 56 trials. are used for statistical analyses, the reported results are based on power estimates that can be considered sufficiently reliable. With respect to the naming of the frequency bands it should be emphasized that the frequency band of 6–8 Hz,

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which is termed ‘‘lower-1 alpha’’, shows only a marginal overlap with the traditional alpha band of 7–13 Hz. However, as the results reported below will show, this frequency band exhibits effects that are quite similar to the lower-2 alpha which ranges from 8 to 10 Hz. As the lower-2 alpha band and in contrast to the theta band, the lower-1 alpha band desynchronizes with increasing task demands. Thus, for simplicity, we use the term lower-1 alpha even for this slow frequency range. This method of adjusting frequency bands individually before analyzing ERD is important because of the following two findings: Ži. alpha frequency varies as a function of several factors such as age, memory performance and attentional demands Žcf. w11,14x and the summary in w8,9x.; Žii. the frequency of the transition region between a taskrelated decrease in band power Žas an indicator for the alpha band. and a task-related increase in band power Žas an indicator for the theta band. shows also a tendency to vary as a function of alpha frequency Žsee e.g. w18x.. It is,

Table 1 Time ANOVA results: Expt. 1, semantic task df Žnumerator. 4 df Ždenom.. 44 Theta F 3.13 e 0.55 Lower-1 alpha F 24.32 e 0.43 Lower-2 alpha F 39.92 e 0.58 Upper alpha F 5.28 e 0.43

b

b

a

Location

Hemi

T=L

T=H

L=H

T=L=H

4 44 2.00 0.41 1.47 0.57 4.00 0.57 11.67 0.59

1 11 0.54 – 1.44 – 1.51 – 2.31 –

16 176 3.62 0.29 2.08 0.13 3.92 0.17 4.60 0.15

4 44 0.17 0.68 0.10 0.43 0.66 0.40 7.63 0.57

4 44 0.90 0.49 0.26 0.63 0.45 0.44 3.20 0.65

16 176 0.95 0.34 2.08 0.32 2.69 0.23 5.15 0.30

a

b

ANOVA results: Expt. 2, free association df Žnumerator. 2 df Ždenom.. 22 Theta F 1.41 e 0.81 Lower-1 alpha F 16.85 b e 0.65 Lower-2 alpha F 12.20 b e 0.78 Upper alpha F 4.65 a e 0.77

4 44 1.28 0.46 1.08 0.57 4.97 a 0.55 7.31 b 0.50

1 11 2.18 – 0.01 – 0.07 – 1.51 –

8 88 4.38 0.47 2.50 0.42 2.67 0.39 3.04 0.36

ANOVA results: Expt. 3, cued recall df Žnumerator. 2 df Ždenom.. 22 Theta F 1.94 e 0.84 Lower-1 alpha F 2.73 e 0.95 Lower-2 alpha F 36.34 e 0.89 Upper alpha F 2.84 e 0.88

4 44 2.73 0.44 1.16 0.55 11.05 0.60 23.83 0.61

1 11 0.00 – 0.91 – 1.25 – 0.34 –

8 88 8.35 0.39 8.52 0.34 3.34 0.35 6.19 0.30

b

b

b

T, time; L, location; H, Hemi Žrecording sites over the left and right sides of the scalp.. a 5%; b 1% level of significance.

b

a

a

b

a

b

b

a

b

2 22 3.96 0.96 0.64 0.82 0.22 0.60 2.40 0.95

2 22 0.02 0.74 0.55 0.79 4.75 0.83 2.86 0.82

b

a

a

a

4 44 0.07 0.62 0.89 0.55 1.98 0.60 3.00 0.54

8 88 0.72 0.42 2.58 0.40 2.59 0.35 3.40 0.31

4 44 1.40 0.75 1.71 0.56 2.59 0.62 4.64 0.59

8 88 1.59 0.38 0.96 0.51 1.63 0.47 2.51 0.42

a

a

b

a

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W. Klimesch et al.r CognitiÕe Brain Research 6 (1997) 83–94

thus, important to use alpha peak frequency fŽi. as a common reference point for adjusting different frequency bands not only for the alpha, but theta range as well. 2.4.5. Statistical analyses Three different types of ANOVAs were calculated. First, 3-factorial ANOVAs were calculated to compare the W1 words of congruent pairs with the W1 words of incongruent pairs of Expt. 1. Second, 3-factorial ANOVAs were calculated for comparisons within each of the three experiments. Third, 4-factorial ANOVAs were computed to analyze effects that are due to differences between the experiments. In order to check whether the W1 words in congruent and incongruent pairs represent homogeneous subsamples, ERD data were subjected to 3-factorial ANOVAs. This was done separately for each of the four frequency bands and for each of the first three time intervals Žt1, t2, t3.. The factors and their levels are: Kong: W1 words of congruent pairs versus W1 words of incongruent pairs; Location: frontal ŽF3, F4, FC5, FC6., central ŽC3, C4, FC1, FC2, CP1, CP2., parietal ŽP3, P4, CP5, CP6., temporal ŽT3, T4. and occipital ŽO1, O2, PO3, PO1, PO2, PO4. leads; and Hemi: recording sites over the left and right Žl, r. side of the scalp. For each of the three experiments and each of the four frequency bands, ERD data were subjected to 3-factorial ANOVAs. The factors are Time, Location, and Hemi. For factor Time the levels are intervals of 500 ms preceding and following the presentation of a word Žt1, t2, t3, t4 and t5 in Expt. 1; t1, t2 and t3 in Expt. 2 and 3.. The levels of Location and Hemi were already described above. The results of the respective ANOVAs are summarized in Table 1. For the analysis of differences between the experiments 4-factorial ANOVAs were calculated for each frequency band. The factors Location, Hemi and Time Žwith only three levels: t1, t2, and t3. were identical with the respective factors of the 3-factorial ANOVAs. The only additional factor is Task Žwith three levels: semantic, free association, and cued recall task.. The Greenhouse–Geisser procedure was used to compensate for violations of sphericity or circularity. For repeated measurement factors with more than two levels, the epsilon factor Ž e . and the adjusted tail probabilities will be reported.

3. Results 3.1. BehaÕioral data In Expt. 1, an average of 5.9% of the responses were incorrect Žyes 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% 3.2. Experiment 1 None of the 12 3-factorial ANOVAs which were calculated to check for differences between the group of W1 words of congruent and that of incongruent pairs showed significant results Žat or beyond the 5% level. in which factor Kong Žeither as main effect or interaction. is involved. This finding demonstrates that the W1 words of congruent and incongruent pairs can be considered a homogeneous sample. Therefore, the data for congruent and incongruent pairs were pooled in all of the analyses reported below. This finding is important because only those W1 words were used in Expt. 2 and 3 which belonged to congruent pairs in Expt. 1 Žsee Section 2.. For the theta band, only one significant result was found as the summary of results in Table 1 shows. Inspection of the respective means of the significant interaction Time = Location reveals that only at occipital recording sites and only during t2 Žstimulus onset of W1. and t4 Žstimulus onset of W2., a pronounced synchronization Žincrease in power. was found. For the lower-1 alpha band the only significant finding is a main effect for Time. The respective means are plotted in Fig. 2 and show a gradual increase in desynchronization from t1 to t5. According to the Scheffe´ test for pairwise comparisons the critical difference at the 5% level is 10.2. As compared to t1, the increase in ERD is significant at and beyond t3. The significant main effect for Time in the lower-2 alpha band shows a similar result Žcf. Fig. 2.. In addition, factor Location Žindicating that the amount of desynchronization is more pronounced at posterior as compared to anterior recording sites. and the interactions Time = Location and Time = Location= Hemi reached significance. The 3-way interaction indicates a left hemispheric advantage Žstronger desynchronization over the left side of the scalp. which can be observed during t2–t4 Žbut not in t1. and which is particularly large at anterior Žincluding temporal. recording sites. For the levels of the significant main effect of Time, the Scheffe´ test for pairwise comparisons yields a critical difference of 10.6 at the 5% level. As compared to t1, the increase in ERD is significant at and beyond t3. In the upper alpha band all but one variance sources reached significance. The significant main effect for Time is depicted in Fig. 2a. The Scheffe´ test for pairwise comparisons yields a critical difference of 18.9 at the 5% level. As indicated by the respective arrow in Fig. 2a, the increase in poststimulus ERD is significant at t5 only. Because the main effects as well as the three significant

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3.3. Experiment 2 The theta band shows two significant interactions, Time = Location and Time = Hemi. Inspection of the respective means reveal a tendency towards an increase of band power Žsynchronization. which is most pronounced at occipital recording sites during t2 Žcf. Fig. 4a.. Hemispheric differences showing a general tendency of an increase in band power in the left hemisphere for all recording sites can be observed during t2 and t3. As in Expt. 1, the only significant finding for the lower-1 alpha band is a main effect for Time. Again, the respective means as depicted in Fig. 2 show a gradual increase in desynchronization from t1 to t3. The Scheffe´ test for pairwise comparisons yields a critical difference of 12.5 at the 5% level Žcf. Fig. 2b..

Fig. 2. Event-related desynchronization ŽERD., reflecting task-related band power changes in the three experiments and the four frequency bands. A significant increase in desynchronization in one of the poststimulus intervals t2–t5 with respect to the prestimulus level of activity t1 is marked by an asterisk. Semantic memory demands are highest in Expt. 1 but during t4 and t5 only. Note that only the upper alpha band responds selectively to this type of task demands.

2-way interactions are included in the 3-way interaction, the description of this result which is depicted in Fig. 3 will suffice to explain all of the remaining significant findings. Fig. 3 shows a pronounced increase in desynchronization Žwhich is much stronger over the left hemisphere. for frontal, central, temporal, and parietal recording sites that can be observed primarily during t5 Ži.e., during the processing of the semantic task.. Most interestingly, the increase in desynchronization from t1 to t5 is significant for all of the five recording locations over the left hemisphere but for none of the right hemisphere. In the right hemisphere, a significant increase was found only from t1 to t4 Žcf. the respective arrows in Fig. 3.. The judgment of a significant increase from t1 to one of the poststimulus intervals t2–t5 is based on the critical difference of 18.9 obtained by the Scheffe´ test for factor Time.

Fig. 3. Event-related desynchronization ŽERD., reflecting task-related band power changes in the upper alpha band at different recording sites over the left and right side of the scalp Ža and b.. The results show a strong left hemispheric advantage Žlarger ERD values over the left as compared to the right hemisphere. particularly during t5. For a better illustration of the complex pattern of laterality effects, the data of a and b are replotted Žin the form: ERD % leftyERD % right. in c. Note the different scale in c.

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In the upper alpha band four of the seven variance sources reached significance. Factor Time reveals a significant increase in desynchronization from t1 to t3 Žthe Scheffe´ test for pairwise comparisons yields a critical difference of 15.7 at the 5% level; cf. Fig. 2b.. Factor Location demonstrates that compared to anterior locations, posterior recording sites exhibit significantly larger ERD values. The 3-way interaction Time = Location= Hemi most interestingly reveals a right hemispheric advantage Žlarger ERD values over the right hemisphere. which is most pronounced at parietal recording sites and which develops during t2 and t3. 3.4. Experiment 3

Fig. 4. In the theta band occipital recording sites show an increase in band power Žnegative ERD values. during the presentation of a word in t2 in all of the three tasks. This effect most likely reflects the occurrence of lambda waves which are known to reflect visual encoding processes. Note that in contrast to Expt. 1 and 2, a tendency of synchronization from t1 to t3 can be observed in the recall task at frontal, central, temporal and parietal recording sites. This finding is in good agreement with a series of results which demonstrate that working memory demands are reflected by a task-related increase in theta band power w16,18x.

For the lower-2 alpha band significant effects were found for Time and Location. These findings demonstrate a significant increase in desynchronization from t1 to t2 and from t1 to t3 Žthe critical difference at the 5% level is 12.8 according to the Scheffe´ test, cf. Fig. 2b. and topographical differences in desynchronization with occipital and parietal recording sites showing the largest degree of desynchronization. Although no further results are significant, it should be noted that the 3-way interaction Time = Location= Hemi Ž F s 2.59; P - 0.075. closely failed to reach the 5% level of significance. Inspection of the respective means yields a pattern of results that is quite similar to the respective findings of Expt. 1: a tendency towards a left hemispheric advantage can be observed during t2 and t3 which is somewhat larger at anterior recording sites.

As in Expt. 1 and 2, the theta band shows a significant interaction between Time and Location. Again, the respective means indicate a pronounced synchronization at occipital recording sites during t2 Žcf. Fig. 4b.. In the lower-1 alpha band the only significant finding refers to the interaction Time = Location. Inspection of the respective means reveal that in contrast to all of the other recording sites, occipital leads show a particularly strong increase in desynchronization from t2 to t3. The lower-2 alpha band shows significant main effects for Time and Location, as well as two significant interactions. For factor Time the Scheffe´ test for pairwise comparisons yields a critical difference of 7.3 at the 5% level Žcf. Fig. 2c.. As in Expt. 2, these findings reflect a significant increase in desynchronization from t1 to t3 Žcf. Fig. 2. and show that occipital and parietal recordings exhibit the largest degree of desynchronization. The interaction Time = Location demonstrates that the increase in desynchronization from t1 to t3 is particularly large at occipital recording sites. In addition, the interaction Time = Hemi reveals a left hemispheric advantage which can be observed during t3 only. For the upper alpha band the significant main effect for Location indicates topographical differences with maximal desynchronization at occipital and parietal recording sites. The significant interaction Time = Location reveals that only occipital and parietal recording sites show an increase in desynchronization from t1 to t3. As in Expt. 2, the interaction Location= Hemi reveals a right hemispheric advantage Žlarger ERD values over the right hemisphere. for parietal recording sites. 3.5. Comparisons between Expt. 1, 2, and 3 with respect to t1, t2, and t3 With the exception of factor Task, the results of the 4-factorial ANOVAs would only repeat findings we already have described above. Thus, only those significant effects will be reported below, in which factor Task is involved.

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For the theta band, interaction Task = Time = Location Ž F16, 176 s 4.37; e s 0.34; P - 0.01. is the only significant finding in which factor Task is involved. The respective means which are plotted in Fig. 4 reveal that in contrast to all of the other recording sites, occipital leads show a pronounced synchronization in the time interval Žt2. immediately following the onset of stimulus presentation. Furthermore, and in contrast to the semantic and the association tasks, the cued recall task shows a consistent tendency of synchronization during t3 at frontal, central, parietal and temporal leads. For the lower-1 alpha band two significant effects with factor Task, interaction Task = Time Ž F4, 44 s 4.21; e s 0.57; P - 0.05. and Task = Time = Location Ž F16, 176 s 3.43; e s 0.23; P - 0.01. were obtained. The respective means of the 3-way interaction Žincluding the 2-way interaction. reveal that the free association task shows Žin

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contrast to the other tasks. a particularly large increase in desynchronization from t2 to t3 at frontal, central, parietal and temporal leads. At occipital recording sites the increase in desynchronization from t2 to t3 is of comparable magnitude for all of the three tasks. Part of this effect Žwith the exception of topographical differences. can be observed in Fig. 2 by comparing the respective differences between t1, t2, and t3. For the lower-2 and the upper alpha band, no significant effects in which factor Task is involved could be obtained. However, for the upper alpha band this negative finding is of particular interest because in the semantic task a significant increase in desynchronization was found during t4 and t5 but not during t1, t2, and t3. In considering the fact that the three tasks do not differ in t1, t2 and t3 suggests that during this time period, no significant desynchronization occurs in the upper alpha band. With respect to the upper alpha band, it should be noted that in contrast to all of the other recording regions, occipital leads show the largest increase in desynchronization over time in all of the three tasks as the respective means of the significant interaction Time = Location Ž F8, 88 s 6.17, e s 0.27, P - 0.01. and the lack of a significant interaction Task = Time = Location of the 4-factorial ANOVA demonstrates. The increase in desynchronization from t1 to t2 at occipital recording sites is 16.8% in the semantic task Žclosely failing to reach significance in the respective 3-factorial ANOVA; cf. Fig. 3., 27.1% in the free association task, and 18.6% in the cued recall task. The fact that the increase in desynchronization from t1 to t2 at occipital recording sites is by far the largest difference that can be observed in the significant interaction Time = Location demonstrates that this topographically highly restricted increase in desynchronization is indeed significant. The respective interaction is plotted in Fig. 5c. In order to illustrate the large differences between the two lower and the upper alpha band, the respective interactions for the lower-1 and lower-2 alpha are plotted in Fig. 5a,b.

3.6. Comparing t4 and t5 of Expt. 1 with t2 and t3 of Expt. 2 and 3

Fig. 5. The topography of desynchronization is strikingly different in the two lower alpha bands as compared to the upper alpha. Whereas band power decreases over time at all of the recording sites in both of the two lower alpha bands, desynchronization is strictly localized at occipital regions in the upper alpha band. The depicted data are averaged over Expt. 1, 2, and 3.

In order to test the hypothesis that the amount of upper alpha desynchronization is significantly larger during t4 and t5 in Expt. 1 as compared to t2 and t3 in Expt. 2 and 3 a 4-factorial ANOVA with the same factors as described in the previous section was calculated. The only difference to the respective ANOVA described earlier refers to factor Time which now has only two levels Žt4, t5 in Expt. 1 and t2 and t3 in Expt. 2 and 3.. In confirming the suggested hypothesis, the main effect for factor Task Ž F2, 22 s 4.48; e s 0.77; P - 0.05. proved to be significant. Furthermore, four of the seven possible interactions including the 4-way interaction Task = Time = Location= Hemi also were sig-

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nificant. This complex pattern of results underlies the findings we already have reported Žcf. particularly the results depicted in Figs. 2 and 3.. We, thus, forgo a further description of these results.

4. 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 Žcf. 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 of significance even before a semantic relationship between the W1 and W2 words can be detected. Thus, when keeping in mind that the semantic task cannot be carried out until the second word W2 of a pair is presented Žduring t4., it becomes evident that only the upper alpha band responds selectively to semantic task demands Žcf. Fig. 2.. The increase in upper alpha desynchronization during the semantic task in t5 is strictly localized over the left hemisphere Žcf. Fig. 3. and is well in line with a variety of PET studies and Tulving’s HERA model w33x. As an example, Petersen et al. w27x have shown that semantic task demands Žparticularly the retrieval of semantic information. are associated with a pronounced increase in the blood flow at left prefrontal regions Žsee also w32x and the review of related findings in w33x.. In addition, Martin et al. w22x have found that naming pictures of animals and tools Žparts of the words used in the present study also represent animals, others such as weapons were similar to tools. was associated with bilateral activation of the temporal lobes and the calcarine region, the left thalamus and the left anterior insularinferior frontal region Žcf. Fig. 1 in Martin et al. w22x.. Desynchronization in the upper alpha band was significantly larger during t4 and t5 of Expt. 1 as compared to t2 and t3 of Expt. 2 and 3. Because semantic memory demands were highest in the congruency task, this finding provides further evidence for the suggested hypothesis that the upper alpha band is associated with semantic memory processes. The upper alpha band, however, not only responds to semantic task demands. Looking at topographical differences reveals that desynchronization is largest at occipital sites during t2 and t4 when the W1 and W2 words are presented Žcf. Fig. 3a,b.. This highly selective increase in desycnchronization most likely reflects visual encoding processes. Furthermore, comparing different recording sites shows an interesting dissociation between different brain areas. Whereas frontal, central, parietal and temporal regions do not respond to the presentation of a word but to

semantic processing demands only, occipital regions respond to both, perceptual and semantic processing demands as the respective findings in Fig. 3 indicate. The processing of perceptual information not only is apparent at occipital recording sites within the upper alpha band but most interestingly in the theta band as well. Inspection of Fig. 4 reveals that in all of the three experiments but only at occipital sites and only during t2 Žand t4 which is not shown in Fig. 4. when a word is presented, a systematic synchronization can be observed. This increase in theta power which is restricted to occipital areas most likely is due to lambda waves which are known to exert maximal power in the theta band w3,4x. According to Billings w4x, lambda waves result from retinal afferents and are observed particularly at occipital regions during the processing of visual information w26x. The two lower alpha bands exhibit similar trends with respect to the time course and topography of desynchronization. Both, the lower-1 and the lower-2 alpha band show a pronounced, gradual increase in desynchronization over time in all of the three tasks Žcf. Fig. 2.. Topographical differences between the two lower and the upper alpha band Žaveraged over Expt. 1, 2, and 3. are depicted in Fig. 5. Whereas the upper alpha band responds with a topographically restricted increase in desynchronization at occipital recording sites during the presentation of a word, the two lower alpha bands exhibit a topographically widespread desynchronization which can be observed before, during, and after a word is presented. Task difficulty tends to be related with the onset of a significant desynchronization in the lower-2 alpha band which occurs already at t2 in the more difficult tasks of Expt. 2 and 3 Žwith an error rate of 13% and 71% respectively; cf. the behavioral data in the Section 3 above., but at t3 in the easy task of Expt. 1 Žwith an error rate of 6%.. The lower-1 alpha band exhibits a similar trend. It is interesting to note that this association between task difficulty and lower alpha desynchronization can be observed despite the fact that the same W1 words were presented in each of the three experiments. The flat topographical distribution of desynchronization of the two lower alpha bands, their generally higher level of desynchronization as compared to the upper alpha band Žcf. Fig. 5a,b in contrast to Fig. 5c. and their relationship to task difficulty support the view that the two lower alpha bands are related to rather unspecific cognitive processes such as general task demands and attention. Thus, the gradual increase in lower alpha desynchronization may reflect the gradual increase in attentional or general task demands from the beginning to the end of a trial. The flat and widespread topographical distribution of lower alpha desynchronization is also well documented by the statistical results which are summarized in Table 1. The upper alpha band shows a total of 10 significant Žout of the 12 possible. variance sources in which factor Location is involved. In contrast to the upper alpha, only six

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significant effects were found for the lower-2 whereas just one effect was obtained for the lower-1 alpha band. Consequently, the upper alpha band yields results that are most sensitive with respect to topographical differences. The most general conclusion that can be drawn on the basis of the reported results is that different cognitive processes are reflected by different and rather narrow frequency bands. This conclusion is well in line with findings of earlier performed studies Že.g. w11–18x.. What is new, however, is the finding that semantic memory as well as perceptual encoding processes are reflected by topographically distinct patterns of desynchronization in the upper alpha. Perceptual processes serve to extract the meaning from sensory information w7x. It, thus, appears likely that upper alpha desynchronization not only responds to verbal-semantic information processing demands Žsuch as those of Expt. 1. but also to any kind of sensory semantic encoding processing.

Acknowledgements This research was supported by the Austrian ‘‘Fonds zur Forderung der wissenschaftlichen Forschung’’ P-11569. ¨ We wish to thank Gernot Florian for his assistance in methodological issues.

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