The effects of ocular artifacts on (lateralized) broadband power in the EEG

Clinical Neurophysiology 112 (2001) 215±231

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The effects of ocular artifacts on (lateralized) broadband power in the EEG Dirk Hagemann a,b,*, Ewald Naumann c a

Laboratory of Personality and Cognition, National Institute on Aging, National Institutes of Health, 5600 Nathan Shock Drive, Baltimore, MD 21224, USA b Department of Psychology, University of Maryland, Baltimore County, MD, USA c Fachbereich I ± Psychologie, UniversitaÈt Trier, Trier, Germany Accepted 30 November 2000

Abstract Objective: Empirical evidence suggests that blinks and eye movements do not generate substantial activity outside the delta and theta range, and that the propagation of ocular activity to the EEG is rather symmetrical. These observations suggest that an alteration of the alpha and beta asymmetry of the EEG due to ocular artifacts is not likely to occur. The aim of the present study is to examine the effects of ocular artifacts on broadband EEG parameters. Methods: EEG and EOG were recorded from 31 participants in a resting condition with eyes open and closed, allowing for spontaneous ocular activity. General effects of ocular artifacts were examined with mean comparisons, and differential effects were examined with correlation analysis of data portions that were selected for a presence or absence of artifacts. Results: At single sites, blinks and eye movements exerted substantial general effects on the whole EEG spectrum, but there were no substantial differential effects of artifacts in the alpha and beta bands, except at the frontopolar sites. The distorting effects of ocular artifacts were smaller in magnitude for asymmetry than for single site measures. Conclusions: The control of ocular artifacts may be dispensable for correlation analyses of alpha or beta band parameters. q 2001 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Electroencephalography; Ocular artifacts; Spectral analysis; Alpha power density; Hemispheric lateralization

1. Introduction The contamination of the electroencephalogram (EEG) with potentials that originate from movements of the eyelid or eyeball are a nuisance for researchers who investigate the electrophysiology of the brain (e.g. Pivik et al., 1993; Picton et al., 2000). The distorting effects of these ocular artifacts on the EEG are very evident in the time domain, and adequate procedures for their control in studies of evoked potentials are indispensable (e.g. Barlow, 1986; Brunia et al., 1989; Gratton, 1998; Picton et al., 2000). However, blinks and eye movements do not generate substantial activity outside the delta and theta range (e.g. Gasser et al., 1985, 1986). Furthermore, electric ®eld potentials decrease with increasing distance to their source (e.g. Nunez, 1981). In addition, the propagation of ocular activity to the EEG appears to be rather symmetrical (e.g. Gasser et al., 1985; van den Berg-Lenssen and Brunia, 1989). The total of these arguments suggests that ocular artifacts are not likely to * Corresponding author. Tel.: 11-410-558-8645; fax: 11-410-558-8108. E-mail address: [email protected] (D. Hagemann).

distort alpha and beta asymmetry in the EEG. The present article reviews the literature that sustains these arguments, and reports on an empirical examination of the effects of blinks and eye movements on the electrooculogram (EOG) and EEG. 1.1. Ocular artifacts in the EEG The cornea of the eye has a positive electric charge compared with the retina, and both structures form an electric dipole. This dipole generates an electric ®eld that propagates across the head, and rotating movements of the eyeballs or lid movements result in alterations of this electric ®eld. In particular, in the vicinity of the eyes at anterior scalp regions, the potentials that are generated by ocular activity interfere with the potentials that are generated by the brain. In consequence, the derivations of the EEG re¯ect neural potentials that are superimposed with ocular potentials or ocular artifacts (for an overview of the generator mechanisms of ocular artifacts, see Elbert et al., 1985; Brunia et al., 1989; Gratton, 1998). Different ocular artifacts may be distinguished (for an

1388-2457/01/$ - see front matter q 2001 Elsevier Science Ireland Ltd. All rights reserved. PII: S 1388-245 7(00)00541-1

CLINPH 2000114

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overview, see Barlow (1986) and the literature cited there). Blink artifacts result from a rapid movement of the eyelid and cause a characteristic peak potential in the spontaneous EEG, with an amplitude of up to 800 mV and a duration of about 200±400 ms. Eye movement artifacts (e.g. saccadic eye movements, smooth-pursuit movements, vertical movements) result from a rotation of the eyeball, and are usually of smaller magnitude but longer duration (Brunia et al., 1989). In addition to their different waveforms in the EEG recordings, blink and eye movement artifacts also show differences in the magnitude of propagation across the scalp, in topography, and spectrum (e.g. Corby and Kopell, 1972; Gratton et al., 1983; Gasser et al., 1985). Since ocular artifacts can be of a much greater amplitude than the neural activity in the EEG, one or another control procedure is obligatory for the analysis of electrical brain activity (Barlow, 1986; Gevins, 1987; Brunia et al., 1989). One common procedure to control for ocular artifacts is the rejection of EEG segments that show contamination with ocular activity (for an overview, see Barlow, 1986). In another approach, ocular activity is removed from the EEG with a regression procedure (for a general overview, see Gratton, 1998). 1.2. The power spectrum of the EOG The spectral composition of different types of eye movements and blinks has been studied with diverse methods for the registration of ocular activity (Whitton et al., 1978; Iacono and Lykken, 1981; Eizenman et al., 1985; Gasser et al., 1985). These studies provided consistent evidence that the mass of power of ocular activity is in the delta (and theta) band, with a sharp and rather monotonous decrease of power with increasing frequency. Based on this evidence, some investigators concluded that the EOG power of eye movements and blinks is negligible in the alpha and beta bands (above 7.5 Hz; e.g. Gasser et al., 1985, 1986). Although corneo-retinal dipole rotations and ocular ®eld alterations due to lid movements are the obvious source of EOG activity, the higher frequency components of the EOG appear to be mostly of neural origin, thus constituting the problem of neural artifact in the EOG. For example, Iacono and Lykken (1981) measured frontal EEG and eye movements during a smooth-pursuit tracking task with EOG and infra-red re¯ectrometry, the latter measuring movements of the eyeball directly. A comparison of EOG and infra-red data revealed a substantial alpha activity (between 7.0 and 13.9 Hz) in the EOG, which was absent in the infra-red data, and thus, suggested a neural origin. This ®nding is in line with reports of Whitton et al. (1978) and Gasser et al. (1985), who presented EOG spectra that showed a protuberance in the alpha band, which resembled the alpha peak in the corresponding EEG spectra. Taken together, these ®ndings suggest that blinks and eye movements generate substantial activity in the delta and

theta bands, but essential portions of the alpha and beta activity in the EOG might be of neural origin. More evidence for the distinction of ocular and neural activity in the EOG stems in particular from studies of the regression approach of artifact compensation. 1 In a frequency domain regression approach, the EOG and EEG is Fourier-transformed into the frequency domain, a regression is performed separately for each frequency component of the EOG and EEG spectrum, and ®nally, the residualized EEG is transformed back to the time domain. The regression spectrum is interpreted as a transmission function and yields a separate transmission coef®cient for each frequency component (for an overview, see van Driel et al., 1989). 1.3. A frequency domain perspective on EOG±EEG transmission In a study of EOG±EEG propagation, Gasser et al. (1985) applied a frequency domain regression approach to their data and presented EOG±EEG transmission functions for data portions of an eyes-closed resting condition. The EOG±EEG transmission functions showed a peak in the theta/alpha range (approximately between 5 and 15 Hz) which was more pronounced for data portions without artifacts compared with the data with artifacts, and that was interpreted as an indication of coherent neural activity. These ®ndings corroborated earlier observations that suggested neural activity in the EOG (Gasser et al., 1983a,b), and were replicated by MoÈcks et al. (1989) and van Driel et al. (1989) who reported on an excessive gain for EOG±EEG transmission in the alpha band. Both author groups suggested that this peak of the transmission functions must be due to coherent prefrontal cerebral activity that was picked up by EOG and EEG electrodes. Commenting on these ®ndings, Berg (1989) also proposed that most of the ocular activity might be below 5 Hz, whereas above 5 Hz, coherent EEG plays the dominant role in the EOG. Similar evidence for a considerable coupling of the EOG and EEG in the alpha range was provided by Whitton et al. (1978) and Waterman et al. (1992). The common conclusion that the EOG activity in the alpha and beta bands is not of ocular origin is also re¯ected by several procedures for the control of ocular artifacts. To account for artifacts for an analysis of spontaneous EEG, Gasser et al. (1983b) selected only segments of the data that showed a minimal EOG power in a frequency band between 1.5 and 7.5 Hz, and a subsequent study suggested that the introduction of further selection criteria did not improve the results (MoÈcks and Gasser, 1984). To account for coherent 1 In a time domain regression approach, a regression of the measured EEG on the measured EOG will yield a residual that is not correlated to the measured EOG and that may be interpreted as the true EEG. The regression weight is interpreted as a transmission coef®cient and quanti®es the fraction of the EOG signal that is propagated to the EEG (for an overview, see Jervis et al., 1989).

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neural activity in the EOG and EEG, Woestenburg et al. (1983) and van Driel et al. (1989) proposed that in the frequency domain regression approach, all transfer coef®cients that exceed a threshold value (and which usually comprise the alpha band) should be set to zero to prevent an over-compensation. Similarly, Waterman et al. (1992) suggested that only the delta band should be used for the frequency domain approach. Likewise, Gasser et al. (1992) proposed a ®ltering of the EOG with a low-pass of 7.5 Hz before the application of a time domain regression approach. In total, these studies strongly suggest that most of the higher frequency range in the EOG is of neural origin, and thus, it may be assumed that ocular activity does not generate substantial power in the alpha and beta bands. The research on the regression approach not only provided considerable insight into the spectral composition of the EOG±EEG transmission, but also offered many ®ndings on the topography of ocular artifacts. 1.4. A topographical perspective on EOG±EEG transmission A simple visual inspection of raw EEG recordings reveals that the size of vertical artifacts like blinks decreases with increasing distance to the frontal poles, and that the size of horizontal artifacts due to eye movements additionally decreases with decreasing distance from the midline (Gasser et al., 1992). This topography is re¯ected by a decrease of the transmission coef®cients/functions from anterior to posterior (e.g. Gratton et al., 1983; Gasser et al., 1985, 1992; Gratton and Coles, 1989; Lutzenberger and Elbert, 1989; MoÈcks et al., 1989; van den Berg-Lenssen and Brunia, 1989; van Driel et al., 1989). Although blinks are usually associated with smaller transmission coef®cients/functions than other types of eye movements (e.g. Corby and Kopell, 1972; Weerts and Lang, 1973; Gratton et al., 1983; Gasser et al., 1985; but see Gratton and Coles, 1989; Kenemans et al., 1991), it generally appears that ocular potentials are attenuated with increasing distance to the eyes. In addition, ocular activity appears to propagate along the anterior±posterior axis in a rather symmetrical fashion. In many reports on time domain regression approaches, the transmission coef®cients of the vertical or horizontal EOG usually showed a highly similar magnitude for contralateral homologous EEG sites, with a similarity somewhat greater for vertical than for horizontal transmission (e.g. Gratton et al., 1983; Gratton and Coles, 1989; Lutzenberger and Elbert, 1989; van den Berg-Lenssen and Brunia, 1989; Gasser et al., 1992). In parallel, applications of the frequency domain approach also provided highly similar transmission functions for the vertical EOG±EEG transfer (Gasser et al., 1985; MoÈcks et al., 1989; van Driel et al., 1989; but see MoÈcks et al., 1989; van Driel et al., 1989). In general, these ®ndings suggest a rather symmetrical propagation of ocular artifacts, which might be explained by the recurrent

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conjugation of the movements and blinks of both eyes (see Gratton, 1998). 1.5. The effects of ocular artifacts on EEG broadband spectral parameters Given the extensive research on procedures for the control of ocular artifacts in the EEG, surprisingly few studies reported on the effects of ocular actions on the power spectrum of the EEG. In an early study on the occipital alpha rhythm, Verbaten et al. (1975) manipulated the amount of eye movements by a rapid visual search vs. a ®xation task, but did not observe a signi®cant change in parieto-occipital alpha activity between these conditions. Unfortunately, EEG was only recorded from the right hemisphere, no anterior EEG sites were included, no other frequency bands were analyzed, and the sample size was limited to 8 participants. Nearly one decade later, MoÈcks and Gasser (1984) recorded EEG in an eyes-closed condition at rest and compared broadband EEG power of the whole, unselected data, including all artifacts, with epochs of 20 s that were individually selected for a minor artifact contamination as indicated by minimal delta and theta power in the simultaneously recorded EOG. A descriptive comparison revealed lesser delta and theta power in the EEG that was selected for the absence of ocular artifacts, in particular, for delta activity at frontal sites. However, there were no substantial differences in alpha and beta powers between these two data selections. The limitations of these ®ndings are due to the procedure for selecting epochs with low artifact contamination, since the 20 s data segments with minimal EOG activity might still contain transient portions with gross artifacts (see the critique of Gasser et al., 1992). Thus, the comparison was probably based on two EEG selections, each containing data with and without gross artifacts, and the effects of ocular activity on EEG broadband power may have been underestimated. In addition, no attempts were made to evaluate the signi®cance of these effects of data selection, and only the data of right hemisphere electrodes were reported. In a similar approach, Gasser et al. (1986) recorded EOG and EEG in a resting state with eyes closed. Among other ®ndings, they presented the EEG broadband power separately for 20 s data segments with minor and major ocular artifact contamination as indicated by minimal and maximal EOG power. On a descriptive level, the EEG portions with minimal EOG power had lower broadband power in the delta and theta bands than the EEG portions with maximal EOG power, in particular, for delta activity at frontal and central sites. At the frontal sites, the power differences in the alpha and beta bands were in the same direction, but rather small in magnitude. Most remarkably, the correlation between the medial frontal EEG power of data selected for minimal and maximal ocular artifacts was low in the delta (0.58), but higher in the theta (0.77), alpha (0.88 and 0.72), and beta (0.86 and 0.88) bands, and these relations

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increased for posterior sites (all r $ 0:89 for all bands at the occipital region). The limitations of these ®ndings are again due to the procedure for selecting epochs with low vs. high artifact contamination (see Gasser et al., 1992), which may have yielded an underestimation of the effects of ocular activity on EEG broadband power, and yet again, no attempts were made to evaluate the signi®cance of these effects of data selection, and no data of contralateral homologous sites were reported. In total, these studies do not provide a ®rm conclusion on the effects of ocular artifacts on alpha and beta band parameters of the EEG, and no cogent inference on the effects of ocular artifacts on EEG asymmetry can be derived from these ®ndings. 1.6. The present study A bulk of evidence implied that ocular artifacts do not generate substantial power in the alpha and beta bands, and that the activity in these broadbands of the EOG is rather of neural origin. However, reliable power in the alpha and beta bands due to ocular activity is a necessary condition for a distortion of spectral parameters in the same bands of the EEG. 2 Furthermore, electric ®eld potentials decrease with increasing distance to their source, thus minor ocular activity in the alpha and beta bands may be attenuated to an insigni®cant magnitude after propagation to the scalp electrodes. In addition, ocular activity is propagated to the EEG in a rather symmetrical fashion, and may result in rather symmetrical distortions of the EEG that leave the true EEG asymmetry unchanged. The main conclusion from the literature is that a distortion of (lateralized) alpha and beta band parameters of the EEG due to ocular artifacts is not likely to occur. On the other hand, all authors commonly concluded that a control of ocular artifacts is indispensable for any analysis of spontaneous background EEG, which is contradictory to the assumed invariance of EEG alpha and beta band parameters. Rather, a lack of distorting effects of ocular artifacts on (lateralized) EEG alpha and beta activity implies that the control of ocular artifacts may be omitted, in particular, if alpha and beta asymmetry is the target of research (for recent examples of such research, see Hagemann et al., 1999; Nitschke et al., 1999; Pauli et al., 1999; Debener et al., 2000). The aim of the present study is to examine the effects of blinks and eye movements on single site and asymmetry broadband spectral parameters of the EEG, and to evaluate the necessity of a control/correction of ocular artifacts for EEG alpha and beta band parameters. Since ocular artifacts (and their potential effects on EEG 2 The (true) EOG time series and the (true) EEG time series have no sinusoidal waveform and can only be represented with broad spectra. The superposition of the (true) EEG time series with the (true) EOG time series must therefore result in an alteration of the power components of the true EEG spectra across a broad frequency range (for a detailed treatment of time series and spectral analysis, see Jenkins and Watts, 1968; Newland, 1993).

alpha and beta activity) are greatest at the anterior electrodes, and since previous studies gave rise to rather paradoxical implications, we included more anterior sites in the present study and conducted more detailed analyses. 2. Methods 2.1. Participants The sample of the present study was drawn from a longitudinal study on brain asymmetry and emotion that was conducted in 1998 at the UniversitaÈt Trier (Germany). The ®rst 31 participants on the ®rst occasion of measurement were subjects of the present study. This sample consisted of 19 female and 12 male students (mean age, 24 years; range, 19±36 years). Prior to the data acquisition, informed consent was obtained from each participant. 2.2. Procedure After arriving at the laboratory, each participant was seated in an electrically shielded EEG cabin and electrodes were applied for the measurement of EOG and EEG. The biosignals were recorded during 12 baseline resting periods (1 min each). Six baselines were recorded with eyes open, and 6 with eyes closed, which constituted a factor Condition (eyes-open, eyes-closed) for later analyses. There was a 1 min break after 4 subsequent baseline recordings. Each participant was randomly assigned to one of two counterbalanced orders of the eyes-open (O) and eyes-closed (C) condition of the resting baselines (OCCO-COOC-OCCO and COOC-OCCO-COOC). The participants were instructed via microphone to be `restful' and when to open and close the eyes. No further instruction to avoid blinking and eye movements was given, and no task to move the eyes was introduced to prevent confounding with task-speci®c brain activity (Gratton et al., 1983; Brunia et al., 1989; Verleger, 1991; Croft and Barry, 1998). The experimenter initiated EOG and EEG recordings of each single baseline after the instruction was given. After the EEG was recorded, the participants completed subsequent tasks that will be reported elsewhere. 2.3. EEG recording and quanti®cation The EEG was recorded with the ECI-Electrocap system (Electro-Cap International, Inc.; Blom and Anneveldt, 1982) from 32 sites of the international 10/10 system (Chatrian et al., 1985), including the earlobes (A1, A2). All sites were referenced to vertex (Cz). A bipolar horizontal EOG was recorded from the epicanthus of each eye, and a bipolar vertical EOG was recorded from supra- and infraorbital positions of the right eye. The EEG was recorded with tin electrodes and the EOG with sintered Ag/AgCl electrodes (Polich and Lawson, 1985). Prior to the placement of electrodes, the expected electrode sites on the parti-

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cipant's scalp and face were cleaned with alcohol and gently abraded. All impedances of the EEG electrodes were below 5 kV, and the differences of impedance of homologous sites were below 1 kV. EEG and EOG were ampli®ed with two 32 channel SynAmps Model 5083 ampli®ers (input impedance, 10 MV; Neuroscan, Inc.) in AC mode. The high-pass frequency was set to 0.3 Hz, and the low-pass frequency was set to 40 Hz to prevent aliasing. The EEG and EOG were digitized at 200 Hz and stored to hard disk for later analysis. After the data acquisition was accomplished, each combined EOG and EEG record was subjected to a visual artifact screening and editing procedure, which resulted in 3 different versions of the edited EEG. For this procedure, the continuous EOG and EEG recordings were visually inspected off-line for the presence of artifacts. Depending on the particular version, portions of the data that showed particular artifacts were rejected for this and all simultaneously recorded channels (for a broad description and classi®cation of artifacts, see Barlow, 1986; Zschocke, 1995). All screening and editing were performed by the ®rst author who has 5 years experience in EEG recording and analysis techniques, and resulted in the following versions of the EEG. 2.3.1. Primary data version Primary In a ®rst step, all non-ocular artifacts were removed from the data. The rejected data were predominately contaminated with muscle, movement or electrode artifacts. This procedure resulted in a version of the data that contained a mixture of spontaneous EEG and ocular artifacts. 2.3.2. Reduced artifact version Noart In a second step, all ocular artifacts were removed from the data of the Primary version. This procedure resulted in a version of the data that was free of overt artifacts. 2.3.3. Only artifact version Onlyart In a last step, the Primary version was edited again, however, this time, all portions of the data that showed no ocular artifacts were removed. This procedure resulted in a version of the data that contained predominately blinks in the eyes-open condition, and mostly eye movements in the eyes-closed condition (a predominance of these ocular artifacts in eyes-open and -closed EEG was previously reported by Gasser et al., 1986). The three data versions constituted a factor, Version (Noart, Primary, Art), for later analyses, with the different factor levels containing either no overt artifacts (Noart), or ocular artifacts of a quantity that represented spontaneous eye activity in a resting situation (Primary), or only overt ocular artifacts (Art). After editing the data, the EOG and EEG were broken down to non-overlapping epochs of 1.28 s. 3 A total of 13 participants had less than 8 epochs (equivalent to 10.24 s of data) in the Onlyart

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Table 1 Summary of EEG version statistics a Condition

Version

N

M

Range

Mean acceptance (%)

Eyes-open

Primary Noart Art Primary Noart Art

31 31 31 31 31 18

253.5 151.8 56.4 261.5 206.5 45.9

171±276 43±248 12±130 181±278 85±275 8±187

90 54 20 93 73 16

Eyes-closed

a N, Number of participants; M, mean; and range of number of epochs available for three artifact versions of the data, separately for the eyes-open and eyes-closed conditions.

version of the eyes-closed condition. These participants were rejected from all subsequent analyses involving this version/condition in order to prevent a reliability drop (Davidson et al., 1990). A description of the resulting version statistics is presented in Table 1. Note that the percentage of accepted epochs of the Noart and Onlyart versions do not add up to the percentage of accepted epochs of the Primary version because data with mediocre or unclear ocular artifacts were not accepted for the Noart or Onlyart versions. Prior to spectral analysis, a computer-averaged ears reference was computed off-line by averaging the A1 ! Cz and A2 ! Cz channels and subtracting this average from the data of the Cz-referenced EEG channels (Davidson, 1988). This procedure prevents a shift of the effective reference site from midway between the ears to the ear with the lower electrode resistance, which may be introduced with a physically linked ear reference and might distort EEG asymmetry (Miller et al., 1991). Separately for the two recording Conditions (eyes-open, eyes-closed) and 3 artifact Versions (Noart, Primary, Art), an odd±even split of the EEG and EOG epochs was performed. This procedure resulted in two parallel data sets for each condition and version and facilitated a reliability analysis of all measures. 4 All epochs were extracted through a Hanning window (10%) to prevent spurious estimates of 3 To measure broad bands with an expansion of only 4 Hz, we planed for a frequency resolution of at least 1 Hz, thus the segment length had to be 1 s or longer. Conversely, we aimed to use as much of the recorded data as possible, and thus wished to use a fairly short segment length (e.g. to capture a rather short EEG portion free of artifacts between two blinks). Since our FFT algorithm requires 2 n data points for each segment and we sampled the data with 200 Hz, we chose a segment length of 1.28 s as a compromise between frequency resolution and data exhaust. 4 A reliability analysis is a helpful prerequisite for the interpretation of a correlation coef®cient, since low reliabilities of variables suppress their correlation. Conversely, a low correlation between two variables may indicate a lack of an essential (true score) relationship between the variables, or a low reliability of one or both variables or a combination of these factors. This ambiguity can be avoided by a reliability analysis and by a correction for attenuation (for further details, see Guilford, 1954).

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spectral power (Dummermuth and Molinari, 1987). A fastFourier-transform (FFT) was performed on all epochs to compute spectral power (mV 2) spaced at intervals of 0.78 Hz. Separately for each condition, version and data set, power values were averaged across the delta (0.5±4 Hz), theta (4±8 Hz), alpha (8±13 Hz) and beta (13±30 Hz) bands and converted to power density (mV 2/Hz; Newland, 1993). Finally, delta power density values were square-roottransformed and the theta, alpha and beta power density values were ln-transformed to normalize the data (see Gasser et al., 1982, for details on these band-speci®c transformations). This procedure resulted in two parallel power density values separately for 4 broadbands, two recording conditions and three artifact versions. To obtain whole power density values for each band, version and condition, each pair of parallel power values was averaged, converted to power density and transformed. Finally, asymmetry measures were computed as the right± left difference of normalized broadband power density between homologues contralateral sites (e.g. ln alpha power density F4 2 ln alpha power density F3; see Davidson, 1988). 2.4. Data analysis The statistical analyses were performed for the two EOG channels and the frontopolar (Fp1, Fp2), lateral frontal (F7, F8), medial frontal (F3, F4), anterior temporal (T3, T4), central (C3, C4), posterior temporal (T5, T6), parietal (P3, P4) and occipital (O1, O2) regions. The effects of ocular artifacts on EEG broadband parameters were analyzed with a set of repeated measures analyses of variance and a set of correlation analyses, with a correction for liberal P values. Prior to further analyses, a reliability check of all measures was completed (a reliability analysis is a helpful prerequisite for the interpretation of a correlation coef®cient, since low reliabilities of variables suppress their correlation. Conversely, a low correlation between two variables may indicate a lack of an essential (true score) relationship between the variables, or a low reliability of one or both variables or a combination of these factors. This ambiguity can be avoided by a reliability analysis and by a correction for attenuation (for further details, see Guilford, 1954)). Separately for each band, version and condition, each pair of parallel power or asymmetry values was correlated, and the Spearman±Brown formula for the reliability of lengthened tests was applied to obtain estimates for the whole power density and asymmetry values (for details, see Guilford, 1954). All EOG measures, all EEG single site and asymmetry measures of the Primary and Noart versions, and the single site measures of the Art eyes-open data showed at least acceptable reliability (range, 0.76±0.99, with the exception of the anterior temporal theta asymmetry of the Noart eyes-open data with a reliability of 0.65). However, the single site measures of the Art eyes-closed data, and all asymmetry measures of the Art version

showed a variety of low and high reliability estimates (range, 0.33±0.99, with the exception of the O2 delta power density which yielded a negative parallel test correlation of 20.06). The reduced reliability of these measures might be due to the limited number of epochs in this particular version (see Table 1). All further analyses were completed with the whole power density values. For a manipulation check and in order to reveal the effects of the amount and type of eye activity on broad frequency bands of the EOG, a Version (Noart, Primary, Art) £ Condition (eyes-open, eyesclosed) analysis of variance of EOG broadband power values was conducted, separately for each frequency band and separately for the horizontal and vertical derivations. The subsequent analyses of the EEG data were performed separately for the eyes-open and eyes-closed conditions to prevent confounding with different brain activities in these conditions. Following Cronbach's (Cronbach, 1957) distinction between experimental and correlational research designs, two statistical types of effects may be distinguished. A general (mean) effect of a manipulation may shift the sample mean of a dependent variable, which thus indicates that all (or most) participants have changed in the same direction (e.g. all participants may show an increased magnitude of that variable due to the manipulation). This type of effect can be examined with methods of mean comparisons like t tests or analysis of variance. In contrast, a differential effect of a manipulation may distort the relative positions of the participants in the sample distribution of a dependent variable, which thus indicates that the participants have changed in different directions (e.g. some participants may show an increased and some participants may show a decreased magnitude of that variable due to the same manipulation). This type of effect reduces the common variance of the variables and can be examined with a correlation analysis. Since an absence or presence of a general (mean) effect does not imply an absence or presence of a differential effect (and vice versa), both effect types have to be analyzed separately. To examine the general (mean) effects of ocular artifacts on EEG activity, a Version (Noart, Primary, Art) £ Hemisphere (left, right) analysis of variance of the broadband power values was performed separately for each frequency band and each of the 8 regions. The resulting effect sizes were quanti®ed with Hays' v 2 (Hays, 1974), which is conceptually comparable to the coef®cient of determination r 2 and quanti®es the portion of the variance of the dependent variable that is due to the variation of the independent variable (see Hays, 1974, and Cohen, 1988, for details). Following a proposal of Cohen (1988), a v 2 of 0.01, 0.06, or 0.14 may be considered to indicate an effect of small, medium or large magnitude, respectively. The differential effects of ocular artifacts on the EEG were examined with correlation analyses of single site and asym-

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metry broadband power density values between the Noart and Primary versions, and between the Noart and Art versions. To prevent a suppression of the correlations involving the Art data as a consequence of low reliability, the Spearman formula for the correction of attenuation was applied to the Noart £ Art correlations (for technical details, see Guilford, 1954). This correction was omitted for the Noart £ Primary correlations because the Noart data was a subset of the Primary data, which violates the assumption of uncorrelated measurement errors. For all effects involving the Version factor, a Huynh± Feldt correction of the degrees of freedom was performed (Vasey and Thayer, 1987). An in¯ation of alpha error probability was prevented by an application of the Bonferoni± Holm correction procedure with a cumulated signi®cance level of 0.05 (Holm, 1979).

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3. Results 3.1. Data description The grand means of power density spectra of the EOG and EEG for the 3 versions in the eyes-open condition are presented in Fig. 1. Across all channels, there was greater power density for the Onlyart than the Primary version and greater power density for the Primary than the Noart version, and this effect of version was greater for the delta and theta bands than for the alpha and beta bands. In particular, this effect of version extended at both EOGs from the lower broadband across the alpha into the lower beta band. For the EEG, the same pattern of power density distribution was present at the frontopolar, lateral frontal and medial frontal sites. However, the graded effect of version was lower in magnitude at the posterior sites, where it already

Fig. 1. Grand means of power density spectra for EOG and EEG channels in an eyes-open resting condition, separately for three artifact versions of the data. N ˆ 31.

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Fig. 2. Grand means of power density spectra for EOG and EEG channels in an eyes-closed resting condition, separately for three artifact versions of the data. N ˆ 31 for no artifacts and primary data version; N ˆ 18 for only artifacts version.

deceased at the lower alpha band. The corresponding grand means for the eyes-closed condition are presented in Fig. 2 and show a similar pattern of power density distribution, although the effects of version are smaller in size and extend only into the lower alpha band at frontal sites and into the theta band at posterior sites. Most remarkably, the Noart power density distribution of the vertical EOG in the eyes-closed condition showed a small protuberance in the alpha band which was hardly visible in the Primary or Onlyart version, and which might correspond to the common alpha peak of the EEG. This interpretation was supported by a correlation analysis of ipsilateral ocular and occipital alpha separately for all three versions. For the Noart condition, right vertical EOG alpha showed a substantial positive relation to O2

alpha (r ˆ 0:42; P ˆ 0:020), whereas the same association was smaller for the Primary version (r ˆ 0:28; P ˆ 0:130) and not present for the Onlyart version (r ˆ 20:03; P ˆ 0:913). Since a contamination of occipital Noart EEG with ocular activity is not likely, the common variance may be explained by a contamination of Noart background EOG with alpha activity of neural origin. 3.2. Manipulation check, and effects of Version on the EOG A Version (Noart, Primary, Art) £ Condition (eyesopen, eyes-closed) analysis of variance with repeated measurement on both factors of EOG broadband power values was conducted separately for each frequency band and separately for the horizontal and vertical derivations.

D. Hagemann, E. Naumann / Clinical Neurophysiology 112 (2001) 215±231 Table 2 Analysis of variance Version (Noart, Primary, Art) £ Hemisphere (left, right) of broadband power density in an eyes-open condition, separately for different regions and frequency bands a

Delta Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2 Theta Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2 Alpha Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2 Beta Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2

Main effect

Interaction

Version

Version £ Hemisphere

F(2,60)

P

v2

P

v2

325.46 248.56 176.83 133.03 85.51 40.56 41.24 45.01

0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0000 b

0.87 0.84 0.79 0.71 0.65 0.46 0.46 0.49

3.85 0.06 6.06 4.84 7.84 2.84 6.47 2.08

0.0573 0.8273 0.0175 0.0228 0.0045 0.0941 0.0120 0.1595

0.03 0.00 0.05 0.04 0.07 0.02 0.06 0.01

207.41 183.83 115.31 65.18 40.21 17.15 18.59 32.41

0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0002 b 0.0001 b 0.0000 b

0.82 0.80 0.71 0.58 0.46 0.26 0.27 0.40

19.03 0.96 9.08 5.69 0.96 4.46 2.86 0.44

0.0001 b 0.3442 0.0025 0.0180 0.3494 0.0316 0.0901 0.5164

0.16 0.00 0.08 0.05 0.00 0.04 0.02 0.00

98.25 83.12 35.96 6.87 2.56 0.21 0.75 0.12

0.0000 b 0.0000 b 0.0000 b 0.0112 0.1156 0.6799 0.4072 0.7632

0.68 0.64 0.43 0.11 0.03 0.00 0.00 0.00

16.48 2.65 6.77 0.28 1.51 0.36 0.41 0.05

0.0001 b 0.1105 0.0097 0.6291 0.2312 0.5719 0.5487 0.8437

0.14 0.02 0.06 0.00 0.01 0.00 0.00 0.00

23.94 24.75 3.70 4.35 1.69 6.71 3.39 11.39

0.0000 b 0.0000 b 0.0585 0.0377 0.2041 0.0116 0.0717 0.0010 b

0.33 0.34 0.05 0.07 0.01 0.11 0.05 0.18

2.00 1.00 0.99 0.26 0.18 0.23 1.23 0.23

0.1648 0.3386 0.3386 0.6501 0.7204 0.6635 0.2807 0.6784

0.01 0.00 0.00 0.00 0.00 0.00 0.00 0.00

F(2,60)

a

Only effects involving Version displayed. Signi®cant with a ˆ 0:05 after the Bonferoni±Holmes correction for 32 simultaneous tests of all main effects or all interaction effects. N ˆ 31. b

Only those effects will be summarized which persisted a Bonferoni±Holm correction for all simultaneous 24 F tests with a ˆ 0:05. For the horizontal EOG, there was a significant main effect of Version for all broadbands (all F …2;34† $ 49:20, all P ˆ 0:0000). For each frequency band, the mean power density was greatest for the Onlyart and smallest for the Noart version, with the Primary version falling in between these values (see Figs. 1 and 2). In addition, the delta band showed the largest and the beta band showed the smallest effect sizes v 2 (delta, 0.85; theta, 0.81; alpha, 0.67; beta, 0.64). None of the main effects of Condition and none of the

223

Version £ Condition interactions were signi®cant (all P $ 0:0356, all v2 # 0:10). For the vertical EOG, there was also a signi®cant main effect of Version for all broadbands (all F…2;34† $ 62:10, all P ˆ 0:0000). Again, the power density was greatest for the Onlyart and smallest for the Noart version, and the delta and theta bands showed the largest and the beta band showed the smallest effect sizes v 2 (delta, 0.89; theta, 0.89; alpha, 0.83; beta, 0.69). In addition, there were signi®cant main effects of Condition for the theta and alpha bands (both F…1;17† $ 19:19, both P # 0:0004). In the eyes-open condition, the participants showed more theta (v2 ˆ 0:37) and alpha (v2 ˆ 0:34) power density in the vertical EOG than in the eyes-closed condition. Finally, there were significant interaction effects of Version £ Condition for all broadbands (all F…2; 34† $ 11:11; all P # 0:0014). For all frequency bands of the Onlyart version, the participants showed more power density during eyes-open compared with eyes-closed, whereas the power density was very similar for both eye conditions of the Noart version (v 2 delta, 0.35; theta, 0.49; alpha, 0.35; beta, 0.16). In summary, the main effects of Version for both the horizontal and the vertical EOG suggest that the intended manipulation of the amount of ocular artifacts between the versions was successful. This manipulation yielded the largest effects in the delta and theta bands, although the considerable effect sizes for the alpha and even the beta band strongly suggest that ocular activity is not only restricted to the lower frequency domain. 3.3. General (mean) effects of Version on the EEG A Version (Noart, Primary, Art) £ Hemisphere (left, right) analysis of variance with repeated measurement on both factors of EEG broadband power values was conducted separately for each frequency band and region for the eyesopen condition. The results of these analyses are presented in Table 2. Only those main effects of Version which persisted a Bonferoni±Holm correction for all 32 main effects with a ˆ 0:05 will be considered as signi®cant, and only those interaction effects which persisted the respective Bonferoni±Holm correction for all 32 interaction effects will be considered as signi®cant. There were signi®cant main effects of Version for all regions in the delta and theta bands, for the frontopolar, lateral frontal and medial frontal regions in the alpha band, and for the frontopolar, lateral frontal and occipital regions in the beta band (all F…2;60† $ 11:39; all P # 0:0010). The effect sizes were greatest for the anterior and smallest for the posterior regions, and greatest for the delta and smallest for the beta band (v 2 range: delta, 0.87±0.46; theta, 0.82±0.26; alpha, 0.68±0.00; beta, 0.34±0.01). For each band at the frontopolar, lateral frontal and medial frontal regions, the power density was greatest for the Onlyart and smallest for the Noart versions, with mean values of the Primary version falling in between (see Fig. 1).

224

D. Hagemann, E. Naumann / Clinical Neurophysiology 112 (2001) 215±231

Fig. 3. Mean broadband power density of frontal sites in an eyes-open condition, separately for Version (Noart, Primary, Art) and Hemisphere (left, right) for different frequency bands with main effect Version removed. N ˆ 31.

In addition, there was a signi®cant Version £ Hemisphere interaction for the theta and alpha power density at the frontopolar region (both F…2;60† $ 16:48; both P ˆ 0:0001). Although the frontopolar interaction effect for the delta band, and the medial frontal interaction effects for the delta, theta and alpha bands were not signi®cant, the respective effect sizes were 0.03 # v 2 # 0.08 and may not be considered as negligible on a descriptive level. Since these interaction effects are relatively small compared with the corresponding main effects of version (see Table 2 and Fig. 1), the frontopolar and medial frontal interaction effects of Version £ Hemisphere were re-plotted for the delta, theta and alpha bands, with the main effect Version statistically removed from the data. The resulting plots are presented in Fig. 3. For the theta and alpha power density at the frontopolar region, the participants in the Noart version showed greater mean right than left asymmetry, whereas for the Primary and, in particular, for the Onlyart version, this asymmetry reverted and the participants showed greater mean left than right power density (theta, v2 ˆ 0:16; alpha, v2 ˆ 0:14). In addition, there was an increase in the frontopolar delta asymmetry (v2 ˆ 0:03), but a decrease in the medial frontal alpha asymmetry (v2 ˆ 0:06) in the Onlyart version compared with the Noart version. The same set of Version (Noart, Primary, Art) £ Hemisphere (left, right) analysis of variance was repeated for the broadband power values of the eyes-closed condition, and the same Bonferoni±Holm procedures were applied. The results of these analyses are presented in Table 3. Again, there were signi®cant main effects of Version for all but the occipital region in the delta band, for the frontopolar, lateral frontal, medial frontal and anterior temporal regions in the theta band, and for the frontopolar region in the alpha band (all F…2;34† $ 11:26; all

P # 0:0021). The effect sizes were also greatest for the anterior and smallest for the posterior regions, and greatest for the delta band and smallest for the beta band (v 2 range: delta, 0.83±0.26; theta, 0.63±0.08; alpha, 0.28±0.00; beta, 0.18±0.01). For each frequency band at the frontopolar, lateral frontal and medial frontal regions, the power density was generally greatest for the Onlyart and smallest for the Noart version, with values of the Primary version falling in between (see Fig. 2). Finally, there was no signi®cant Version £ Hemisphere interaction for any of the broadbands and regions (all P $ 0:0262; all v2 # 0:08). However, the interaction effect sizes for the frontopolar theta (v2 ˆ 0:05) or alpha (v2 ˆ 0:08) power density may not be considered as negligible. For both frequency bands at these sites, the participants showed greater mean right than left asymmetry in the Noart version, whereas for the Onlyart version, this asymmetry was reverted (the respective plot was omitted due to space limitations). Taken together, the main effects of Version suggest that there are substantial general effects of ocular artifacts on mean EEG power density across all frequency bands. The interaction effects of Version £ Hemisphere were relatively small in size, which suggests that the distortion of the EEG by ocular activity occurred mostly in a symmetrical manner. Nonetheless, these interaction effects were substantial at the anterior region and indicated unsystematic distortions of theta and alpha asymmetry. 3.4. Differential effects of Version on the EEG A correlation analysis of single site broadband power density values and asymmetry measures between the Noart and Primary versions and between the Noart and Art versions was conducted separately for each frequency

D. Hagemann, E. Naumann / Clinical Neurophysiology 112 (2001) 215±231 Table 3 Analysis of variance Version (Noart, Primary, Art) £ Hemisphere (left, right) of broadband power density in an eyes-closed condition, separately for different regions and frequency bands a

Delta Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2 Theta Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2 Alpha Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2 Beta Fp1, Fp2 F7, F8 F3, F4 T3, T4 C3, C4 T5, T6 P3, P4 O1, O2

Main effect

Interaction

Version

Version £ Hemisphere

F(2,34)

P

v2

F(2,34)

P

v2

64.43 132.66 62.85 101.05 38.41 22.49 17.56 10.72

0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0000 b 0.0001 b 0.0004 b 0.0038

0.71 0.83 0.70 0.79 0.58 0.44 0.38 0.26

0.77 0.03 0.16 2.20 0.23 0.38 0.68 0.29

0.4085 0.8991 0.7162 0.1511 0.6602 0.5654 0.4487 0.6239

0.00 0.00 0.00 0.02 0.00 0.00 0.00 0.00

34.08 47.04 16.22 23.07 9.89 5.46 8.19 3.27

0.0000 b 0.0000 b 0.0003 b 0.0001 b 0.0041 0.0283 0.0084 0.0835

0.55 0.63 0.36 0.45 0.25 0.14 0.21 0.08

3.89 0.46 1.16 0.07 0.08 0.57 0.87 0.04

0.0461 0.5564 0.3096 0.8113 0.8098 0.4772 0.3704 0.8828

0.05 0.00 0.00 0.00 0.00 0.00 0.00 0.00

11.26 9.15 3.23 4.02 2.33 0.84 0.46 0.16

0.0021 b 0.0058 0.0855 0.0585 0.1428 0.3770 0.5192 0.7046

0.28 0.23 0.08 0.10 0.05 0.00 0.00 0.00

5.50 2.77 1.27 0.08 0.55 3.91 5.36 2.76

0.0262 0.1088 0.2763 0.7995 0.4850 0.0628 0.0309 0.1109

0.08 0.03 0.00 0.00 0.00 0.05 0.07 0.03

1.68 6.92 1.39 3.90 3.28 3.81 3.16 3.98

0.2122 0.0150 0.2605 0.0635 0.0784 0.0633 0.0890 0.0576

0.02 0.18 0.01 0.10 0.08 0.09 0.07 0.10

0.87 1.23 2.16 0.10 0.61 0.92 0.54 0.02

0.3682 0.2864 0.1577 0.7609 0.4546 0.3548 0.4838 0.9042

0.00 0.00 0.02 0.00 0.00 0.00 0.00 0.00

a

Only effects involving Version displayed. Signi®cant with a ˆ 0:05 after the Bonferoni±Holmes correction for 32 simultaneous tests of all main effects; none of the interaction effects persisted this correction. N ˆ 18. b

band, region and eye condition. The results of this analysis are presented in Table 4. For the eyes-open condition, the association between single site measures of the Noart and Primary delta power density was low or mediocre in magnitude across the whole scalp without regional speci®city (0.16 # r # 0.72), whereas the correlations between the theta power density of both versions were low for anterior but high for posterior regions (0.28 # r # 0.99). In the alpha band, both versions showed a mediocre association for the frontopolar region (left, r ˆ 0:70; right, r ˆ 0:71), but a great relationship for the rest of all scalp regions (0.93 # r # 0.99), and there was a great association

225

between both versions for the beta band across the whole scalp (0.98 # r # 0.99). The association between Noart and Art power density showed a similar pattern of broadband and regional speci®city, but was generally smaller in size (delta, 0.01 # r # 0.47; theta, 0.21 # r # 0.97; alpha, 0.77 # r # 0.94, except the frontopolar region with r ˆ 0:50; beta, 0.93 # r # 0.98). All r $ 0:58 were signi®cant in this analysis after a Bonferoni±Holm correction for all 128 tests. This analysis was supplemented by a corresponding correlation analysis of asymmetry measures for the eyes-open condition (see Table 4). The associations of asymmetry between the versions showed a similar pattern as was noted for the single site analyses with one notable exception. The relations of delta asymmetry between both versions were greater than the corresponding relations for the single sites. Between the Noart and Primary versions, there was a mediocre or great association for the delta and theta asymmetry, with lower correlations for anterior and higher correlations for posterior regions (delta, 0.41 # r # 0.94; theta, 0.31 # r # 0.94). The alpha asymmetry was strongly related between both versions for the whole scalp (0.88 # r # 0.99), except the frontopolar region (r ˆ 0:58), and there was a great association between versions for the beta asymmetry across the whole scalp (0.97 # r # 0.99). The correlation analysis between Noart and Art asymmetry yielded a similar association pattern, but smaller relations for anterior sites (delta, 0.35 # r # 0.94; theta, 0.12 # r # 0.99; alpha, 0.69 # r # 0.99, except the frontopolar region with r ˆ 0:38; beta, 0.91 # r # 0.99). All r $ 0:55 were signi®cant in this analysis after a Bonferoni±Holm correction for all 64 tests. These correlation analyses were repeated with single site and asymmetry measure for the eyes-closed condition (see Table 4). Between the single site measures of the Noart and Primary versions, there were mediocre or great associations for the delta band across the whole scalp (0.64 # r # 0.92), and great relations for the theta band with lower correlations for anterior and higher correlations for posterior regions (0.85 # r # 0.99). For the alpha and beta bands, all correlations between both versions of all regions showed a size of 0.99. The associations between Noart and Art power density showed a similar pattern, but were smaller in magnitude (delta, 0.02 # r # 0.57; theta, 0.40 # r # 0.99; alpha, 0.94 # r # 0.99; beta, 0.75 # r # 0.99). All correlations of the Noart £ Primary analysis and all r $ 0:69 of the Noart £ Art analysis were signi®cant after a Bonferoni±Holm correction for all 128 tests. The corresponding correlation analysis of the asymmetry measures between the Noart and Primary versions showed mediocre or great relations for the delta and theta bands (delta, 0.59 # r # 0.93; theta, 0.71 # r # 0.93), great relations for the alpha band (0.82 # r # 0.96), and mediocre or great relations for the beta band (0.59 # r # 0.98). There was no regional speci®city of these associations. Finally, the

226

D. Hagemann, E. Naumann / Clinical Neurophysiology 112 (2001) 215±231

Table 4 Correlations of single site and asymmetry broadband power density between 3 artifact versions of the data in two recording conditions. All correlations of single site measures in the eyes-closed condition between the Noart £ Primary version and all respective correlations between the Noart £ Art version with r $ 0:69 are signi®cant after a Bonferoni±Holmes correction for all 128 two-tailed t tests with a ˆ 0:05. All correlations of asymmetry measures in the eyesclosed condition between the Noart £ Primary version and all respective correlations between the Noart £ Art version with r $ 0:68 are signi®cant after a Bonferoni±Holmes correction for all 64 two-tailed t tests with a ˆ 0:05. Recording condition

Eyes-open

Eyes-open a

Eyes-closed a,b

Eyes-closed a

Noart £ Art b,c

Edition combination

Noart £ Primary

Broadband

Delta

Theta

Alpha

Beta

Delta

Theta

Alpha

Beta

Delta

Theta

Alpha

Beta

0.72 0.68 0.60 0.32 0.27 0.52 0.64 0.17 0.14 0.46 0.43 0.16 0.12 0.44 0.39 0.72

0.30 0.28 0.49 0.54 0.58 0.46 0.81 0.76 0.81 0.85 0.85 0.84 0.87 0.92 0.84 0.99

0.70 0.71 0.93 0.97 0.98 0.96 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.98 0.99 0.98

0.98 0.98 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99

0.44 0.38 0.32 0.18 0.19 0.23 0.47 0.08 0.05 0.28 0.33 0.04 0.01 0.31 0.26 0.39

0.23 0.21 0.37 0.44 0.46 0.36 0.67 0.54 0.62 0.70 0.72 0.66 0.72 0.82 0.64 0.97

0.50 0.50 0.77 0.85 0.87 0.84 0.93 0.90 0.90 0.94 0.88 0.89 0.90 0.92 0.88 0.87

0.93 0.90 0.93 0.98 0.97 0.96 0.98 0.97 0.96 0.97 0.95 0.98 0.96 0.96 0.98 0.96

0.67 0.72 0.75 0.64 0.67 0.82 0.67 0.69 0.71 0.81 0.84 0.77 0.82 0.91 0.92 0.89

0.85 0.87 0.87 0.96 0.98 0.95 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99

0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99

0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99 0.99

0.41 0.69 0.42 0.78 0.74 0.94 0.90 0.72

0.37 0.31 0.55 0.79 0.94 0.91 0.93 0.40

0.58 0.88 0.95 0.98 0.99 0.98 0.97 0.98

0.99 0.98 0.99 0.99 0.97 0.99 0.98 0.99

0.35 0.65 0.14 0.68 0.44 0.94 0.47 0.68

0.39 0.12 0.22 0.51 0.95 0.93 0.99 0.21

0.38 0.69 0.86 0.99 0.99 0.89 0.91 0.87

0.99 0.95 0.95 0.94 0.90 0.98 0.91 0.98

0.82 0.93 0.80 0.82 0.61 0.59 0.79 0.88

0.88 0.72 0.86 0.71 0.81 0.88 0.76 0.93

0.85 0.82 0.82 0.87 0.92 0.91 0.96 0.91

0.98 0.59 0.82 0.97 0.74 0.96 0.69 0.97

Single derivations Fp1 Fp2 F7 F3 F4 F8 T3 C3 C4 T4 T5 P3 P4 T6 O1 O2 Asymmetry Fp2-Fp1 F8-F7 F4-F3 T4-T3 C4-C3 T6-T5 P4-P3 O2-O1

Noart £ Art

Noart £ Primary

Delta 0.21 0.37 0.22 0.11 0.13 0.38 0.47 0.26 0.14 0.57 0.45 0.19 0.12 0.46 0.36 0.02 d 0.68 0.74 0.24 0.45 2 0.06 0.29 0.68 0.99

Theta

Alpha

Beta

0.49 0.52 0.40 0.69 0.79 0.55 0.94 0.95 0.95 0.96 0.99 0.99 0.98 0.99 0.99 0.99

0.95 0.94 0.98 0.98 0.98 0.96 0.97 0.99 0.99 0.98 0.98 0.98 0.97 0.97 0.97 0.97

0.94 0.88 0.91 0.97 0.99 0.89 0.82 0.99 0.99 0.75 0.97 0.98 0.99 0.98 0.98 0.96

0.84 0.29 0.76 0.99 0.89 0.92 0.95 0.99

0.79 0.96 0.86 0.88 0.99 0.92 0.99 0.93

0.90 0.42 0.88 0.96 0.84 0.99 0.99 0.96

a

N ˆ 31. With Spearman correction for attenuation. c N ˆ 18. d The parallel test correlation for O2 delta power density was 20.06 and the Spearman correction was omitted. All correlations of single site measures in the eyes-open condition with r $ 0:58 are signi®cant after a Bonferoni±Holmes correction for all 128 two-tailed t tests with a ˆ 0:05. All correlations of asymmetry measures in the eyes-open condition with r $ 0:55 are signi®cant after a Bonferoni±Holmes correction for all 64 two-tailed t tests with a ˆ 0:05. b

association between Noart and Art asymmetry measures showed a similar pattern (delta, 0.29 # r # 0.99, except the central asymmetry with r ˆ 20:06; theta, 0.76 # r # 0.99, except the lateral frontal asymmetry with r ˆ 0:29; alpha, 0.93 # r # 0.99, except the frontopolar asymmetry with r ˆ 0:79; beta, 0.84 # r # 0.99, except the lateral frontal asymmetry with r ˆ 0:42). All correlations of the Noart £ Primary analysis and all r $ 0:68 of the Noart £ Art analysis were signi®cant after a Bonferoni±Holm correction for all 64 tests. In summary, the rather low correlations between the delta and theta measures of the 3 versions, but the high correlations of the alpha and beta measures, suggest that the differential effect of ocular activity on single site and asymmetry measures is mainly restricted to the lower frequency bands. In these bands, the differential effects of ocular artifacts

were smaller in magnitude for asymmetry measures than for single site measures. 4. Discussion The present study demonstrated that blinks and eye movements do generate substantial activity in the whole spectrum of the EOG, including the alpha and beta bands. Accordingly, this ocular activity exerted substantial general effects on the whole spectrum of the EEG at single sites and resulted in an artifactual increase of the mean broadband power, including the alpha and beta band parameters of the anterior scalp region. However, the differential effects of ocular artifacts were less pronounced. Although blinks and eye movements severely distorted the sample distribu-

D. Hagemann, E. Naumann / Clinical Neurophysiology 112 (2001) 215±231

tion of EEG activity in the delta and theta bands, the differential effects of ocular artifacts were negligible in the alpha and beta range, with the exception of the frontopolar sites. Furthermore, the distorting general and differential effects of ocular artifacts appeared to be much smaller in magnitude for asymmetry than for single site measures. In marked contrast to the conclusions of previous studies, the present results not only suggest large general effects of artifacts on the alpha and beta bands, but also that there are well-de®ned EEG paradigms, like the analysis of individual differences in anterior alpha asymmetry, for which an elaborate control of ocular artifacts may be dispensable. In the following sections, each of these ®ndings will be discussed in detail. 4.1. Effects of blinks and eye movements on the EOG In general, the spectra of the EOG showed their mass of power in the delta (and theta) band, whereas the power in the alpha and beta bands was relatively small in magnitude, which replicates previous evidence (Whitton et al., 1978; Iacono and Lykken, 1981; Gasser et al., 1985, 1986). Furthermore, vertical and horizontal EOG segments that were selected for high ocular activity, like blinks or eye movements, showed more power density across the whole spectrum (from 0.5 to approximately 20 Hz) than EOG segments that were selected for an absence of ocular activity; EOG derivations that were contaminated with a mediocre amount of ocular activity fell in between both extreme selections. Similar to the results of Gasser et al. (Gasser et al., 1985, 1986), this effect was greatest for the delta and theta bands. In contrast to previous ®ndings, this effect extended for both EOGs across the alpha and into the beta band, where it was still very large in magnitude with respect to Cohen's (Cohen, 1988) convention for effect sizes (e.g. there was a main effect of ocular activity on the horizontal EOG alpha power density at a size of v2 ˆ 0:67, and the corresponding effect size for the vertical EOG alpha power density was even v2 ˆ 0:83). Most importantly, this ®nding suggests that eye movements and blinks not only generate considerable activity in the delta and theta bands, but also in the high-frequency broadbands. Complementing these ®ndings, segments of the vertical EOG in the eyes-closed condition that were selected for an absence of ocular activity showed a small protuberance in the alpha band, which is similar to ®ndings of Whitton et al. (1978) and Gasser et al. (1985). This protuberance was neither visible in the segments that were selected for the presence of ocular artifacts, nor was it visible in the eyesopen condition. Since neural alpha activity is greater during eyes-closed than eyes-open (e.g. Shagass, 1972), this ®nding suggests that the protuberance resembles the common alpha peak in the EEG, and thus, is of neural origin. In addition, for the eyes-closed data that were selected for an absence of ocular artifacts, there was a substantial positive association between the alpha power density of the vertical EOG and the ipsilateral occipital alpha power density,

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whereas the same association was smaller for the EOG± EEG data that were contaminated with a medium amount of ocular activity, and it was not present for the data portions that were selected for the presence of gross ocular artifacts. Since a contamination of occipital EEG with ocular artifacts is particularly unlikely for an EEG that was selected for an absence of ocular activity, this ®nding renders further support for the assumption that the EOG alpha activity during the absence of ocular activity is of neural origin. These ®ndings suggest a two-fold nature of the alpha and beta activity in the EOG, which profoundly revises the widespread assumption that this high-frequency range is, in general, dominated by neural activity (for such a common suggestion, see Whitton et al., 1978; Woestenburg et al., 1983; MoÈcks and Gasser, 1984; Gasser et al., 1985; Gasser et al., 1986, 1992; Jonkman et al., 1986; Berg, 1989; MoÈcks et al., 1989; van Driel et al., 1989; Waterman et al., 1992; Gratton, 1998). In the absence of blinks and eye movements, the low-amplitude EOG background activity in the alpha and beta bands is most likely of neural origin. However, during the presence of blinks and eye movements, the high-amplitude EOG shows an associated activity in the broadband between 0.5 and 20 Hz that appears to be mainly of ocular origin, and the respective high-frequency components of the EOG signals might result from the non-sinusoidal wave-shape of blinks and eye movements. In this process, the alpha and beta activity of neural origin is probably too small in size to persist a superposition with the relatively greater alpha activity due to blinks and eye movements. 4.2. Effects of ocular activity on single site EEG 4.2.1. General (mean) effects Blinks and eye movement artifacts resulted in severe alterations of mean EEG broadband parameters in all frequency bands, which resembled the effects of ocular activity on the EOG spectra. In the delta and theta bands, segments that were selected for a severe contamination with ocular artifacts showed greater power density at all sites of the scalp than EEG segments that were selected for an absence of ocular artifacts. This effect was greater for the delta than the theta band, greater for anterior than posterior sites, and greater for blinks in an eyes-open condition than for eye movements in an eyes-closed condition. The EEG data that were contaminated with a mediocre amount of ocular artifacts fell in between both extreme selections. In total, these ®ndings replicate previous results (MoÈcks and Gasser, 1984; Gasser et al., 1986), and are in line with ®ndings on the effects of artifact compensation procedures (Gasser et al., 1986, 1992; Waterman et al., 1992). In contrast to previous reports, the EEG segments that were selected for the presence of ocular artifacts showed greater power density in the alpha and beta bands than segments without artifacts, although this effect was restricted to anterior sites. This effect was greater for the

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alpha than for the beta band, and also greater for blinks than for eye movements. Most importantly, the corresponding effect sizes clearly suggest that the general effect of ocular artifacts on anterior EEG activity in the alpha and beta range is of a very large magnitude (e.g. the main effect of ocular activity on the medial frontal alpha power density showed effect sizes of v2 ˆ 0:43 for eyes-open and v2 ˆ 0:08 for eyes-closed). Possibly, prior research did not notice this effect because no anterior sites were included in the analysis (Verbaten et al., 1975), or because a sub-optimal separation of data fragments with or without artifacts was conducted (MoÈcks and Gasser, 1984; Gasser et al., 1986; see Gasser et al., 1992). The distorting impact of blinks and eye movements on the high-frequency activity of the EEG may be explained by the substantial ocular activity in the higher frequency range as was unexpectedly revealed in the present study. Although the EOG power density appears to be small in the highfrequency bands compared with lower bands, ocular dipoles generate more powerful electric potentials than the brain. Thus, even the relatively small fraction of ocular activity that resides in the high-frequency range may be much larger in magnitude than the neural activity in the same band. In consequence, the ocular activity may still exceed the neural activity in the alpha and beta bands even after propagation across the head, and thus a superposition of both activities would increase the sample mean of the parameter. It is only in the posterior region where the ocular activity in the higher frequency range is attenuated by propagation to such a degree that no sizable distortions of the corresponding EEG activity occur. 4.2.2. Differential effects The differential effects of ocular artifacts on lowfrequency activity at single sites were similar to the corresponding general effects. In the delta and theta bands, a severe contamination of EEG with ocular artifacts resulted in substantial distortions of the participants' positions in the sample distribution; again, this effect was greater for the delta than the theta band, greater for the anterior than the posterior sites, and greater for blinks than eye movements. In parallel, a mediocre contamination resulted in lesser, but still considerable, alterations of individual differences. For the alpha and beta bands, however, the differential effects of ocular artifacts appeared to be rather negligible. In the alpha band, the only considerable differential effect of ocular artifacts was limited to the frontopolar sites. All other sites showed no substantial differential effects under this condition (e.g. the correlation of medial frontal alpha power density between data that were selected for the absence of ocular artifacts and unselected data was at least 0.97 across hemispheres and conditions). Furthermore, any differential effects of ocular artifacts were virtually absent in the beta band. Across the whole frequency range of interest, these ®ndings resemble the results reported by Gasser et al. (1986). In total, the differential effects of ocular artifacts appeared

to be smaller in magnitude than the general effect of artifacts. This ®nding suggests that interindividual differences of ocular activity are rather small compared with intraindividual variations of ocular activity across different states of blinks, eye movements, and their absence. In consequence, individual differences in blink and eye movement activity only exerts a distorting effect of the EEG sample distribution in the delta and theta bands where the EOG power density is maximal, and, in particular, at anterior sites that are proximal to the eyes. 4.3. Effects of ocular activity on lateralized EEG 4.3.1. General (mean) effects In the eyes-open condition with its predominance of blinks, ocular artifacts resulted in unsystematic alterations of mean asymmetry in the delta, theta, and alpha bands, although these effects were considerably smaller in magnitude than the corresponding effects of ocular activity on single sites, and exceeded a conservative criterion for significance only in the theta and alpha bands at frontopolar sites. The eye movements in the eyes-closed condition exerted a similar pattern of effects that was even smaller in magnitude and not signi®cant. These ®ndings render some support for the assumption that ocular artifacts would result in rather symmetrical distortions of EEG spectra across the whole frequency range of interest, and are in line with previous reports on rather symmetrical transmissions of ocular activity to the EEG sites (e.g. Gratton et al., 1983; Gasser et al., 1985, 1992; Gratton and Coles, 1989; Lutzenberger and Elbert, 1989; MoÈcks et al., 1989; van den Berg-Lenssen and Brunia, 1989; van Driel et al., 1989). Nonetheless, the effect sizes for asymmetrical distortions were substantial for many sites on a descriptive level, particularly in the theta and alpha bands (e.g. there was an interaction effect between blink activity and hemisphere on the medial frontal alpha power density at a size of v2 ˆ 0:06 in the eyes-open condition, which may be considered to be of medium magnitude according to conventional criteria). This ®nding corresponds to previous reports on asymmetrical EOG±EEG transfer above approximately 5 Hz (MoÈcks et al., 1989; van Driel et al., 1989), and may be explained by systematic asymmetries of anatomy, and general asymmetries in ocular activity (Lutzenberger and Elbert, 1989; MoÈcks et al., 1989). 4.3.2. Differential effects The distorting effects of ocular artifacts on individual differences of asymmetry measures were substantially smaller in the delta and theta bands than the corresponding alterations of the single site measures (e.g. the mean correlation via Fisher's Z-transform of delta power density at single sites between data segments that were selected for the absence and presence of mediocre artifacts was 0.45 across the scalp, but the corresponding mean correlation for delta asymmetry was 0.75). This observation is also in

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line with the assumption that ocular artifacts are propagated in a rather symmetrical fashion. Nonetheless, the differential effects on low-frequency asymmetry were still substantial in magnitude, which suggests a considerable disparity of ocular effects from perfect symmetry. For the higher frequency bands, however, a sizeable differential effect on alpha asymmetry was again limited to the frontopolar sites only. There was no substantial discrepancy between differential effects on single site and asymmetry measures for the remaining scalp regions (e.g. the correlation of alpha asymmetry between data segments that were selected for the absence and presence of mediocre ocular artifacts was 0.95 for the medial frontal region in the eyes-open condition). This ®nding may be merely explained by the absence of differential effects of ocular activity on single site measures in the high-frequency bands. To sum up, the distortions of asymmetry due to ocular artifacts appeared, in general, to be much smaller in magnitude than the corresponding effects for single site measures. This observation may be explained by the rather symmetrical nature of most ocular activities. Nonetheless, the general effects of blinks on asymmetry in the delta, theta and alpha bands were still substantial in size. However, the differential effects on asymmetry measures in the alpha and beta bands followed approximately the corresponding low effect sizes for single sites, and were thus largely negligible. 5. Conclusions The ®ndings of the present study may have several practical implications for spontaneous EEG research. First, the need to control ocular artifacts in mean comparisons of alpha and beta band parameters may have been underestimated in previous research (e.g. Woestenburg et al., 1983; van Driel et al., 1989; Gasser et al., 1992; Waterman et al., 1992). A substantial body of evidence suggests that there are reliable group differences and cognitive or affective task variations in eye movement and blink frequency (e.g. Fogarty and Stern, 1989; Gasser et al., 1992; Stern, 1992). In conjunction with the present ®ndings of very large distortions due to general effects of ocular artifacts in all broadbands, these reports suggest that ocular artifacts may mimic general (mean) EEG power differences between groups and tasks, not only in the delta and theta range, but equally well in the alpha and beta bands. Thus, an appropriate control of ocular artifacts appears to be indispensable for mean comparisons in all frequency bands. Second, the use of the regression approach for artifact compensation may be discouraged if anterior alpha (and presumably beta) activity is the target of research. The validity of this approach is crucially dependent on the assumption that there is no brain activity in the EOG data, or otherwise these procedures would give biased results, and thus, introduce a secondary artifact (Berg, 1989; Gratton and Coles, 1989; Jervis et al., 1989; McCallum and Pocock, 1989;

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MoÈcks et al., 1989; Pham, 1989; van den Berg-Lenssen and Brunia, 1989; van Driel et al., 1989; Berg and Scherg, 1994). No matter how sophisticated the procedures for the estimation of the transmission coef®cients/functions are, or if these procedures were explicitly designed to account for coherent EOG±EEG activity (e.g. Gratton et al., 1983; Gasser et al., 1986), the actual correction of the data is accomplished by a simple subtraction of a fraction of the EOG from the EEG. Thus, if the EOG contains neural activity, then this neural activity is removed from the EEG. Previous ®ndings and the present study demonstrated the presence of alpha activity in the EOG. Therefore, neural alpha activity at anterior EEG sites may be distorted by this procedure. 5 Finally, the absence of differential effects of ocular artifacts in the alpha and beta bands suggests that the need to control blinks and eye movements for any quantitative analysis of EEG parameters may have been overemphasized (e.g. Barlow, 1986; Pivik et al., 1993). With the exception of the frontopolar region, the correlations of alpha and beta power density at all sites were at least 0.93 between unselected data and data selected for the absence of artifacts, which implies that the control procedure is rather needless. In general, these ®ndings suggest that a control of ocular artifacts for a correlation analysis of single site and asymmetry measures in the alpha and beta bands might be dispensable. Although Gevins (Gevins, 1987, p. 39) suggested that `it is neither sensitive nor correct to apply elaborate computer analyses to data contaminated with artifacts', this comment appears to be an overstatement in light of the present ®ndings.

Acknowledgements The authors are grateful to Drs Melissa H. Kitner-Triolo and John J. Sollers III for helpful comments on an earlier version of the manuscript, Renate Freudenreich, Alexander LuÈrken, and Helmut Peifer for technical support, Hannes Ruge for software writing, and Sabine Christ, Johannes Hewig, and Elke Stephan for data acquisition. Portions of this work were presented at the 24th Meeting of the Deutsche Gesellschaft fuÈr Psychophysiologie und ihre Anwendungen (German Society for Psychophysiology and its Applications) in LuÈbeck, Germany, June 1998, and the 38th Meeting of the Society for Psychophysiological Research in Denver, September 1998. This research was supported by the Deutsche Forschungsgemeinschaft 5 To counteract this nuisant effect of the regression approach, Gasser et al. (1992) proposed a low-pass ®ltering of the EOG with a low-pass of 7.5 Hz before the application of the regression procedure. Although this ®ltering certainly prevents the distortion of EEG alpha and beta due to neural activity in the EOG, such a ®ltering would also remove all ocular activity in the alpha and beta bands from the EOG, which, in turn, may prevent an effective removal of ocular activity in these frequency bands from the EEG. Whether ®ltered or not, the bene®t of the regression approach for frontal alpha and beta activity appears to be questionable.

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