Using resting state EEG to investigate long-term stability in children’s frontal EEG alpha asymmetry
by Barbara C.N. Müller1 & Markus Paulus2
1Behavioural Science Institute, Radboud University Nijmegen, The Netherlands
2Ludwig-Maximilians University Munich, Germany
Address correspondence to:
Barbara Müller, Behavioural Science Institute, Radboud University Nijmegen, P.O. Box 9104, 6500 HE Nijmegen, The Netherlands,
phone: +31(0)24 361 59 44, fax: +31(0)24 361 26 77, e-mail: B.Muller[at]bsi.ru.nl
In a recent study (Müller, B. C. N., Kühn-Popp, N., Meinhardt, J., Sodian, B., & Paulus, M. 2015. Long-term stability in children’s frontal EEG alpha asymmetry between 14-months and 83-months. International Journal of Developmental Neuroscience, 41, 110-114), we measured resting state alpha EEG in children at two measurement points.
Neuroimaging research demonstrated that frontal EEG asymmetry in the alpha frequency band (the relative difference between activity recorded from the left frontal scalp locations and the corresponding right locations) is an important marker for individual differences in emotion regulation, affective style, and motivational processes in adults and children (e.g., Buss et al., 2003). For example, Fox and colleagues (1995) showed that 4-year-old children’s frontal asymmetry was related to their social competence in peer interactions. More recently, research demonstrated that relatively stronger left frontal cortical activation in a resting state at 14 months predicted infants’ empathic reactions to others in pain at 24 months (Paulus et al., 2013).
Several studies suggest that frontal alpha asymmetry reflects stable characteristics over time both in different age groups of adults (e.g., Tomarken et al., 1992) and children (Jones et al., 1997). For example, Jones and colleagues (1997) reported stability in frontal asymmetry across a 24-30 months interval in early childhood (age three to six years at baseline), and Vuga and colleagues (2008) across a 6-36 months interval in early childhood (age three to five years) and school children (age six to nine years). Less is known about parietal- and temporal alpha asymmetry. Parietal asymmetry has been connected to differences in brain development (e.g., Anokhin et al., 2000), and shown to be stable in school children (age six to nine), but not in early childhood (age three to five).
Due to the tight interrelation between frontal asymmetry and social behaviour, it is interesting to learn more about the developmental stability of individual differences in frontal asymmetry from early infancy to early childhood. In the present study, we assessed resting state EEG at two measurement points: at 14 months and at about 7 years (i.e., almost 6 years later) after they entered elementary school. At both ages, we analysed asymmetry in the alpha band at frontal, temporal, and parietal sites.
Participants consisted of children who participated in an on-going longitudinal study (Licata et al., 2014). The final sample consisted of 18 children (N = 9 female). Children’s mean age at the first EEG session was 13.99 months (range = 13.67 – 14.43) and at the second session 82.63 months (range = 80.23 – 87.70). Seventeen children were reported to be right-handed, one child to be left-handed. All parents gave written consent after being informed about the procedure, both before the first and second EEG session.
Both EEG recording sessions – the 14 months- and the 83 months visit – were situated in an electrically-shielded, sound-attenuated chamber with a 19-inch computer monitor placed 100 cm in front of the participants.
For the 14 months-visit baseline EEG was recorded while the infant sat quietly on the mother’s lap. During EEG recording, brightly coloured bubbles were presented. This procedure allowed to keep the infant’s visual attention and to yield minimal eye and motor movements. The presentation endured at least 3 minutes and was stopped when the infant lost interest in the stimulus, indicated by yawning, strong motor activity, or crying. Mothers were instructed not to talk to infants during the EEG recording.
For the 83 months-visit, the EEG data were collected while the children were sitting in an armchair. Eight 45 seconds resting baseline periods with eyes-open (O) or eyes-closed (C) were presented. For the eyes open condition, participants were verbally instructed (via sound files at 65 dB SPL) to look at a blue fixation cross presented against a black monitor background; for the closed eyes condition, instructions were to sit comfortably with their eyes closed. These two conditions were presented in alternating order beginning with the eyes-open condition (O, C, O, C, O, C, O, C) with a pause of 7 seconds in between. Due to comparability of the procedures, we focussed on the open-eyes condition to assess longitudinal relations between the two measurement points. Stimulus presentation was controlled via the Presentation software package (Neurobehavioral Systems).
EEG was registered with Cz reference via BrainAmp amplifier (Brain Products, Gilching, Germany) and active Ag/AgCl electrodes (actiCAP, Brain Products, Germany). The band-pass filter settings were 0.016 to 100 Hz and the sampling rate was 500 Hz. Impedance of all electrodes were kept below 10 kΩ. For infants (at 14 months) seventeen sites (Fp1, Fp2, F3, F4, F7, F8, F9, F10, C3, Cz, C4, T7, T8, P3, P4, O1, O2) were placed according to the International 10/20 System at locations commonly used in infants EEG research. Fp1 and Fp2 were used to obtain eye blinks and vertical eye-movements; F9 and F10 allowed to detect horizontal eye-movements as well as to assess frontal activation asymmetries. For children (83 months) the EEG was recorded from 64 sites, which were placed on standard positions of the extended International 10/20 System. The vertical electrooculogram (EOG) was recorded from an electrode placed below the right eye (VEOG) and F9 and F10 was used to detect horizontal eye-movements and assessed frontal activation asymmetries.
EEG data analysis
EEG data were examined and analysed using BrainVision Analyzer 2 (Brain Products, Germany). All channels were re-referenced to a whole-head average reference and digitally band pass filtered with 1 – 20 Hz. Subsequently, the data were segmented into epochs of 1 s with 50 % overlap. By means of semi-automatic artifact rejection and visual inspection, segmented epochs were identified as artifacts and excluded if EEG amplitude of any channel exceeded ± 120 µV for infants (14 months) and 100 µV for children (83 months), or if they contained eye-movements, blinks or (motor) artifacts. For the 14 months olds, on average, 44.7% of all epochs were eliminated from subsequent analyses, resulting in about 294 (SD = 111.8) epochs per infant. For the 83 months olds data were time locked to the four open eyes trials. The segmentation resulted in 356 epochs. After artifact rejection on average 41.0 % were eliminated from subsequent analyses, resulting in about 210 (SD = 50.2) epochs per child. Artifact-free epochs were extracted through a Hanning window and power spectra were calculated via Fast Fourier Transform (FFT) and expressed as mean square microvolts (µV²). For the 14 months olds power was computed for the 6 – 9Hz frequency band, corresponding to the alpha band in adults. For the 83 months olds the 8 – 13 Hz frequency band was computed. To normalize the distribution, EEG alpha power was natural logarithm-transformed. EEG alpha asymmetry scores were calculated as the difference between natural logarithm of EEG alpha power at the right recording site and the left recording site. That is, the asymmetry score for the frontal sites (AsymF) was computed by subtracting the average ln left power (F9, F7, F3) from the average ln right power (F10, F8, F4). Similarly, asymmetry scores for temporal sites (AsymT) and parietal sites (AsymP) were calculated by subtracting left power (T7) from right power (T8) and (P3) from (P4) respectively. Sites were chosen based on earlier research investigating resting state asymmetries (Fox et al., 1992; Vuga et al., 2006; Vuga et al., 2008).
Table 1 presents the mean values and standard derivations for alpha asymmetry scores at the first visit (14 months) and the second (83 months) visit.
Table 1: Pearson correlations between frontal (AsymF), temporal (AsymT), parietal (AsymP) alpha asymmetry scores as well as asymmetry scores of individual frontal electrodes (F3-4, F7-8, F9-10) at 14 months of age (first visit) and frontal (AsymF), temporal (AsymT), parietal (AsymP) asymmetry and asymmetry scores of individual frontal electrodes (F3-4, F7-8, F9-10) scores at 83 months of age (second visit).
Pearson product correlations were calculated between the asymmetry scores (AsymF, AsymT, AsymP) at 14 months and at 83 months of age. Missing data were pairwise deleted. Results demonstrated significant positive relations between frontal asymmetry scores at 14 and 83 months of age (r(18) = .638 p < .004, Figure 1).
Figure 1: Scatter plots of EEG resting state activation between 14-months (x-as) and 83-months (y-as) for the frontal asymmetry.
This effect remains highly significant while controlling for the age range at the second visit (r(18) = .639, p < .006, df = 15). However, no stable relations between the two measurements for temporal and parietal sites were found (Table 2), even if controlled for age.
Table 2: Alphaasymmetry mean values and standard derivations at 14 months of age (first visit) and at 83 months of age (second visit).
The current study investigated the stability of frontal, temporal, and parietal resting state asymmetry from infancy till the early school years. Across an interval of 69-months, evidence for frontal asymmetry stability was found, while no relationship occurred for temporal and parietal sites, even after controlling for age range. These findings extent earlier research demonstrating stable frontal alpha asymmetry in infants and children across 2-4 years (e.g., Kim & Bell, 2006) by showing a stable relationship of frontal alpha asymmetry across a period of nearly six years. The present study is, to the best of our knowledge, the first assessing alpha asymmetry stability across early childhood, between infancy and school age.
Given the widespread changes in cortical organization during early childhood (Thatcher et al., 1987), the present findings are of special interest for the use of frontal alpha asymmetry measures to investigate processes underlying emotion and motivation in childhood. They further advance our understanding of trait implications of alpha asymmetry during early development. Our findings suggest individual differences in brain functioning found as early as 14 months show a remarkable high stability across early childhood.
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