Biological Psychology 85 (2010) 258–267

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Biological Psychology
journal homepage: www.elsevier.com/locate/biopsycho

Developmental aspects of language lateralization in delta, theta, alpha and beta

EEG bands
Chiara Spironelli a , Alessandro Angrilli a,b,∗
a
University of Padova, Department of General Psychology, 35131 Padova, Italy
b
CNR Institute of Neuroscience, 35121 Padova, Italy

a r t i c l e i n f o a b s t r a c t

Article history: This study aimed to clarify the functional role of several EEG bands across age by analyzing language hemi-
Received 12 February 2010 spheric lateralization in three linguistic tasks. Twenty-eight children, 22 young adults and 20 middle-aged
Accepted 16 July 2010 participants were administered the same sample of written words and normalized amplitudes of ␦, ϑ,
Available online 24 July 2010
␣ and ␤ bands were analyzed. Only young adults showed rightwards lateralization in ␦ frequency band.
Task-dependent right-lateralization marked adults’ ϑ and ␣ distributions, whereas only linguistic vs.
Keywords:
non-linguistic differences were found in children. Concerning the high-beta band, all groups showed
Spectral analysis
left-lateralized linguistic effects. In adults slow rhythms represent indices of active inhibition of task-
Aging
Development
irrelevant regions, but in children they marked incomplete automated linguistic processing. The high-beta
Hemispheric lateralization band revealed task-relevant left hemisphere linguistic activity in all groups, therefore representing the
Phonological processing most reliable EEG marker of language hemispheric dominance in children and adults.
Semantics © 2010 Elsevier B.V. All rights reserved.

1. Introduction the insular cortex). Indeed, results obtained by studies on lan-

Language is a feature which typically distinguishes humans
from animals and is associated with specific hemispheric lateral-
ization (Crow, 2004). Indeed, the functional lateralization of the
human brain appears necessary for the full realization of the lin-
guistic potential (Geschwind and Galaburda, 1985; Hiscock, 1998;
Luria, 1973; Pulvermüller, 2001). Results achieved by functional
Magnetic Resonance Imaging (fMRI), Positron Emission Tomogra-
phy (PET) or functional Trans-Cranial Doppler (fTCD) imaging have
clearly demonstrated that the most steady laterality effects are reli-
ably located over the left inferior frontal areas (e.g., Benson et al.,
1999; Démonet et al., 1994; Deppe et al., 2000; Frith et al., 1991;
Liotti et al., 1994; Petersen et al., 1988; Rutten et al., 2002; Xiang
et al., 2010; Zatorre et al., 1992). However, in their review Fiez
and Petersen (1998) identified a complex neural network which
selectively involves not only specific regions within the left hemi-
sphere (e.g., the ventral occipito-temporal cortex, the fusiform and
lingual gyri, and the frontal operculum, among others), but also
some important areas distributed in both hemispheres (e.g., the
anterior/posterior portions of the superior temporal gyrus, the dor-
sal/ventral portions of the postcentral gyrus, the basal ganglia and
∗ Corresponding author at: University of Padova, Department of General Psychol-
ogy, via Venezia 8, 35131 Padova, Italy.
Tel.: +39 049 8276692; fax: +39 049 8276600.
E-mail address: alessandro.angrilli@unipd.it (A. Angrilli).
guage development have suggested that brain plastic mechanisms
involved in linguistic learning are different from those recruited
later for automated, skilled language. For example, one 10-year
longitudinal study (Stiles et al., 2002) on children suffering from
pre- or peri-natal focal brain injury showed that linguistic learn-
ing includes a cortical network which becomes redundant once
the learning is complete—a process which largely takes place in
the early phases of language development. Thus, the achievement
of the typical left hemisphere specialization for linguistic func-
tioning can only be attained once early critical stages of learning
are completed. Concerning written language, Bakker (1979, 2006)
carried out a series of ERP studies on word reading in young read-
ers with limited linguistic competence, and suggested that early
phases of learning to read are mediated by a strategy which mainly
involves the right hemisphere. When children gradually develop
more complex writing skills, reading strategies change accordingly:
advanced readers show a shift from the right to the typical left
dominance (Bakker, 1979). Thus, speech and comprehension are
complete in infants and children (Dehaene-Lambertz et al., 2010;
Friederici et al., 2007), as both these skills start to develop since
the first year of age, whereas the capacity for writing and read-
ing at this age is significantly delayed and not yet fully developed.
Indeed, the study of Grossi et al. (2001) which aimed at analyzing
the developmental aspects of language lateralization during writ-
ten word reading in different age groups (ranging from 7 to 23
years), showed that the left lateralization of the Contingent Neg-
ative Variation (CNV), a slow wave elicited by a S1–S2 paradigm,

0301-0511/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.biopsycho.2010.07.011
 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
increased linearly with age until 19–20 years. In a previous study
on the developmental dynamics of the N150—recognition potential
(Spironelli and Angrilli, 2009a), we found a lack of left hemisphere
linguistic dominance in children also in the early automatic phases
of word recognition.
Despite their low spatial resolution, electroencephalography
and magnetoencephalography provide very accurate temporal res-
olution and allow the identification of the cortical activity which
can be time- or phase-locked to a stimulus or task, for example by
means of evoked potential analysis. Another approach consists of
the analysis of oscillatory characteristics of the signal by means, for
example, of time-frequency methods. Thus, it is possible to describe
EEG in terms of its frequency components – which range from 1
to 100 Hz – over two main functional ranges, that is low frequency
bands (delta: 0.5–4 Hz; theta: 4–8 Hz; alpha: 8–13 Hz), ascribed the
broad functional role of cortical inhibition to slow rhythms (e.g.,
Adrian and Matthews, 1934; Pfurtscheller et al., 1996), and high
frequency bands (beta: 13–30 Hz; gamma: 30–100 Hz), associated
with cortical activation and neural networks integration (e.g., Ray
and Cole, 1985; Steriade, 2000). Recent studies have, however, sug-
gested a re-evaluation of the functional interpretation of EEG bands.
For example, von Stein and Sarnthein (2000) have claimed that,
with the exception of the delta rhythm, all other bands mark differ-
ent levels of cortical, top-down integration. Palva and Palva (2007)
came to the same conclusions, and suggested that alpha, beta and
gamma bands are complementary and coexisting rhythms which
are necessary to the unification process of high level cognitive
operations associated to cognitive demands. Whereas the func-
tional meaning of high frequency bands, such as beta and gamma
rhythms, is unanimously accepted, depending on the experimen-
tal paradigm, as a marker of cognitive processing, integration and
learning (e.g., Jensen et al., 2007; Miltner et al., 1999; Tallon-
Baudry and Bertrand, 1999; Weiss and Rappelsberger, 1998), low
frequency bands, such as theta and alpha, have been recently asso-
ciated with either working memory engagement (Bastiaansen et
al., 2002; Scheeringa et al., 2009; for a review, see Klimesch, 1999)
or active inhibition of task-irrelevant cortical regions (for a review,
see Klimesch et al., 2007). Concerning the delta frequency, this slow
rhythm is typically observed in the deepest stages of sleep and is
strongly reduced during adults’ awake states (e.g., Steriade, 2000).
In addition, when it appears in wakefulness, the delta activity is
considered a marker of brain damage or pathological conditions
resulting from neurological damage or psychiatric disease (e.g.,
Babiloni et al., 2006; De Jongh et al., 2001; Penolazzi et al., 2008;
Spironelli and Angrilli, 2009b; Tanaka et al., 1998; Vieth et al., 2001;
Wienbruch et al., 2003).
A few studies have investigated EEG bands across age, with
a developmental approach. Indeed, the progressive increase in
beta power in individuals aged from 7 to 60 years was associ-
ated with the parallel decrease in alpha and theta power (Anokhin
et al., 1996). Age dependent fine-grained differences have been
found for theta activity, in children ranging from 6 to 11 years of
age (Yordanova and Kolev, 1997) and, for the EEG alpha band, in
young adults compared with middle-aged participants at frontal
sites (Kolev et al., 2002). However, to our knowledge, no EEG
research has been carried out on functional and developmental
aspects of linguistic hemispheric specialization for written word
processing. Thus, the present study aimed at investigating the elec-
trophysiological correlates of reading mechanisms in school-age
children, and the changes associated with a progressive reading
skill development in young and middle-aged adults. Indeed, it is
not clear whether competent 10-year-old readers have developed
a full left hemisphere specialization for written words and, at the
same time, whether middle-aged adults maintain the same left
hemisphere linguistic dominance with respect to younger adults.
A second, important aim was to investigate whether, among all
259
EEG bands, there is a rhythm which can reflect the specialized
left hemisphere linguistic networks necessary for an efficient, yet
not perfect, reading, in school-age children. A related scientific
question arises regarding the possible degradation of left linguistic
networks due to normal aging. Therefore, based on our previously
validated paradigm (Penolazzi et al., 2008; Spironelli and Angrilli,
2006, 2009b; Spironelli et al., 2006, 2008), we carried out a spec-
tral FFT analysis on the same sample of 10-year-old children, young
adults, and middle-aged participants used in our previous work on
early ERP components (Spironelli and Angrilli, 2009a). The analysis
of a large number of EEG bands allowed us to clarify the func-
tional role of low and high frequency bands in different age groups
using the same experimental paradigm and tasks. Indeed, children’s
frontal lobes are not mature and fully myelinizated yet, and this
would be detected by slow frequency bands. In addition, left frontal
areas are important organizers of the whole language (Bookheimer,
2002, Hagoort, 2005) and these are expected to be less lateral-
ized in children. In detail, we expected: (1) in accordance with
the maturational lag hypothesis (e.g., Harmony et al., 1990), that
children show higher delta amplitude than adults, particularly in
the left anterior regions involved in linguistic processing and inte-
gration (Bookheimer, 2002; Hagoort, 2005; Xiang et al., 2010); (2)
that children have greater left hemispheric theta and alpha ampli-
tude compared with adults, since linguistic processes underlying
written word reading are not entirely automated in 10-year-old
readers, and the adopted paradigm is suited to load the verbal
working memory (Angrilli et al., 2000; Klimesch, 1999; Spironelli
and Angrilli, 2006; Spironelli et al., 2006, 2008); (3) that both adult
groups exhibit higher levels of theta and alpha rhythms in right
vs. left hemisphere, especially during the phonological processing
which requires an active inhibition of contralateral, non-linguistic
regions (Klimesch et al., 2007; Spironelli and Angrilli, 2006); (4) that
adults have overall greater beta band percentage than children, and
show greater left vs. right hemisphere lateralization especially in
the Phonological task.
2. Methods
2.1. Participants
Twenty-eight children (14 girls; mean age: 10.01 years, SD: ±0.18 years), 22
young adults (11 females; mean age: 22.59 years, SD: ±3.67 years) and 20 middle-
aged participants (7 females; mean age: 59.10 years, SD: ±7.11 years) entered the
experiment. All subjects were native Italians fully right-handed (on average above
90% according to the Edinburgh Handedness Inventory; Oldfield, 1971), and had
normal or corrected-to-normal vision. None of the participants had been treated
for any neurological or psychiatric disorder, nor were they under pharmacological
treatment at the time of the experimental session.
All adults and children’s parents gave their written informed consent to the
study, according to the Declaration of Helsinki. The experimental procedures were
approved by the Ethics Committee of the Faculty of Psychology, University of Padova.
2.2. Stimuli, tasks, and procedure
The stimuli consisted of bi- or trisyllabic Italian content words, selected from
a frequency dictionary of 5000 written Italian words (Bortolini et al., 1972). Words
were visually presented in pairs on a 17 computer monitor, one at a time with an
intertrial interval of 3 s. The first word (W1) remained on the screen 1.5 s for children
and 1 s for both adult groups. After a fixed interstimulus interval of 2 s, the second
word (W2) was presented until the participant responded by pressing a keyboard
button, but for an interval no longer than 5 s. Word pairs were administered in three
separate blocks corresponding to three tasks, in which the same words were pre-
sented as W1, but in a different randomized order. In the Phonological task, upon
W2 target presentation, participants had to decide whether word pairs rhymed; in
the Semantic task, whether target word W2 was of the same semantic category as
W1; in the Orthographic task (used as control), whether word pairs were written in
the same case (see Spironelli et al., 2006, 2008, for details of the whole experimen-
tal procedure). Therefore, both Phonological and Semantic tasks required different
levels of linguistic processing, whereas the Orthographic control task requested a
simple visuo-perceptual word matching, since the linguistic access was not neces-
sary. To perform motor responses, participants used their left index or middle finger
for pressing two keyboard buttons corresponding to match-mismatch conditions.
Each task included 80 trials/word pairs. In all tasks, 50% matches were randomly
260 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267

interspersed with 50% mismatches. The task order was randomly varied across par-
ticipants. Since we used the same sample of words as W1 in all tasks, we can expect
that any statistical differences found between tasks (including the interaction of task
with the other factors) are due only to the specific processes engaged by the task
itself and not to possible confounding factors differing between samples of stimuli, a
problem that often raises in experimental designs using different samples of stimuli
for different tasks. In addition, we administered one task at a time: this experimen-
tal strategy stimulated participants to process the first word (W1) depending on
the specific linguistic process required by the task and to keep the critical linguistic
features in the working memory until the second word (W2) appeared. In support
of this choice, we have demonstrated in a number of past studies with both ERPs
and EEG bands that both W1 and ISI elicit linguistic task-related reliable (and cross-
linguistic) effects (Angrilli et al., 2000; Mondini et al., 2008; Spironelli and Angrilli,
2006, 2007, 2009a, 2009b; Spironelli et al., 2006, 2008, 2010, in press).
At the beginning of the experiment, all participants were administered a direct
Digit Span (DS) test in order to verify the extent of their verbal short-term memory.

2.3. Data acquisition and analysis

EEG was recorded by 38 tin electrodes; 31 mounted on an elastic cap (Elec-

troCap) according to the International 10–20 system (Oostenveld and Praamstra,
2001). The other 7 electrodes were applied below each eye (Io1, Io2), on the two
external canthi (F9, F10), nasion (Nz) and the mastoids (M1, M2). All cortical sites
were on-line referred to Cz as this site is located at the topographical center of the
scalp and is not used for analysis of lateralization. Data were off-line re-referenced
to the average reference: this solution allowed us to analyze, in addition to all
other important linguistic sites, the mastoid-temporal lobe activity. Data were
stored using the acquire software NeuroScan 4.1 version (NeuroScan Labs, Sterling,
USA). Amplitude resolution was 0.168 ␮V/bin; the bandwidth ranged from DC to
100 Hz (6 dB/octave). The sampling rate was set at 500 Hz and impedance was kept
below 5 K.
Behavioral measures collected from each subject included error rates (ERs) and
response times (RTs) to the second stimulus. EEG was continuously recorded in DC
mode and stored for later analysis. After the completion of the data collection, the
EEG signal was corrected for blinks and eye movement artifacts (according to Ille
et al., 2002) by BESA software (Brain Electrical Source Analysis, 5.1 version). Each
EEG trial epoch was divided into four 1024-ms time intervals, and thus included
512 samples with 0.98 Hz FFT resolution. Each interval corresponds to a different
word processing phase required by the task: 1024 ms before W1 onset (Baseline);
1024 ms after W1 onset (Word 1, W1); the first second after W1 offset, i.e., from
1500 to 2524 ms for children and from 1000 to 2024 ms for both adult groups (Ini-
tial Inter Stimulus Interval, iISI); the last second after W1 offset (before W2 onset),
i.e., from 2476 to 3500 ms for children and from 1976 to 3000 ms for both adult
groups (Terminal ISI, tISI). These time windows were selected on the basis of previ-
ous studies (Penolazzi et al., 2008; Spironelli et al., 2006, 2008). Given the constraint
of the Fast Fourier Transform (FFT) to use 2n samples, the width of each interval
was necessarily forced to 512 samples, corresponding to a 1024-ms interval. The ISI
therefore contained a very small overlap (48 ms, <5%) between iISI and tISI. This par-
tial overlap was a consequence of the decision not to change the main parameters of
our validated paradigm on language lateralization (a solution which allowed us to
analyze, in prior research, also evoked potentials). However, the possible problem
related to the small overlap among time intervals is further limited by the win-
dowing which cancels out the contribution of the extreme portions of the intervals.
Artifact rejection was performed on each epoch, with both amplitude and deriva-
tive (with respect to time) thresholds1 (150 ␮V and 100 ␮V/ms, respectively). The
remaining epochs were then visually inspected for any residual artifacts. On aver-
age, 15% of the trials were rejected for children, 7% for young adults and 12% for
middle-aged participants, evenly distributed across tasks. For each participant, and
for each interval of interest, the FFT was averaged across those epochs which, after
windowing with a tapered cosine, were free of residual artifacts (i.e., on average
68 epochs for children, 74 epochs for young adults and 70 epochs for middle-aged
participants). The last step was the percentage-normalization of EEG amplitudes
within each electrode: this normalization is a scaling procedure which allows to
compare subjects with very different total spectral power, and was calculated as
the contribution of each band to the whole 0.98–100 Hz spectral range,2 expressed
as a percentage (see also Fig. 1; in detail, normalization was computed as the sum of
spectral points of the selected band divided by the sum of all spectral points within
1
Using BESA software, artifact rejection includes an Amplitude threshold cri-
terion, that rejects each trial within which the difference between the maximum
and the minimum amplitude is exceeded, and a Derivative threshold criterion, that
rejects every trial within which the largest amplitude difference between two adja-
cent time samples is exceeded.
2
Preliminary analyses revealed a Gaussian distribution in all groups (mean,
median, skewness and kurtosis have been controlled for each EEG band) and the
percentage-normalization procedure of EEG bands did not affect the normal dis-
tribution of EEG data. Of course, this transformation makes each EEG rhythm not
completely independent from the others; however all data are described and dis-
cussed, thus allowing a comprehensive view of all bands.
Fig. 1. Contribution of each EEG band, ranging from low-delta to high-gamma
frequencies, across the normalized EEG spectrum (0.98–100 Hz) in children
(left column), young adults (central column) and middle-aged participants
(right column). ␦ = delta rhythm; ϑ = theta rhythm; ␣ = alpha rhythm; ␤1 = low-
beta rhythm; ␤2 = high-beta rhythm; ␤3 = beta/gamma rhythm; ␥1 = low-gamma
rhythm; ␥2 = high-gamma rhythm.
the 0.98–100 Hz range). Depending on the rationale of our paradigm, which was
aimed to measure language lateralization, the percentage-normalization allowed
us to compare the same scalp locations in all samples and, at the same time, to
quantify the relative contribution of each EEG band with respect to total spectral
power (therefore as a percentage) in different age groups (Fig. 1): a strategic choice
useful for measuring laterality phenomena in a developmental perspective. To avoid
the 50 Hz noise artifact, the frequency lines corresponding to the interval between
47.9 and 51.8 Hz (three samples) were eliminated. The delta band3 (1–4 Hz, effective
␦ range: 0.98–3.91 Hz), theta band (4–8 Hz, effective ϑ range: 4.88–7.82 Hz), alpha
band (8–13 Hz, effective ␣ range: 8.79–12.72 Hz), and beta band (divided in low-beta
or ␤1: 13–20 Hz, effective ␤1 range: 13.68–20.52 Hz; as well as the high-beta band
or ␤2: 21–28 Hz, effective ␤2 range: 21.49–28.33 Hz), were analyzed. The gamma
band (divided into low-gamma or ␥1: 35–50 Hz, effective ␥1 range: 36.15–47.87 Hz;
and high-gamma or ␥2: 50–65 Hz, effective ␥2 range: 51.78–65.46 Hz) and other
high frequency bands (i.e., 80–100 Hz, effective range: 80.11–99.65 Hz) completed
the whole EEG spectrum (Fig. 1), but were not included in the present statistical
analysis, which considers only conventional EEG spectral bands. As in our previous
study, for statistical purposes, electrodes were clustered into four groups/regions
of interest with two spatial factors consisting of two levels each: antero-posterior
asymmetry and laterality (Spironelli et al., 2006). Each quadrant therefore com-
prised the averaged amplitude of four electrodes: anterior left (AL: F3, FC3, F7, FT7),
anterior right (AR: F4, FC4, F8, FT8), posterior left (PL: P3, P7, M1, O1), and pos-
terior right (PR: P4, P8, M2, O2). Since preliminary analyses carried out for each
EEG band revealed no effects susceptible to the time course, we decided to col-
lapse the three time intervals following the first word onset (i.e., W1, iISI and tISI
intervals) by computing their mean amplitude. This solution was aimed to increase
the statistical power and improve data presentation making result interpretation
easier.
The analysis of Variance (ANOVA) was carried out on the dependent variable
Digit Span including the between-subjects factor Age (three levels: Children vs.
Young vs. Middle-aged). With regard to behavioral measures (mean ERs and RTs),
ANOVA included the between-subjects factor Age (three levels: Children vs. Young
vs. Middle-aged) and the within-subjects factor Task (three levels: Orthographic vs.
Phonological vs. Semantic).
On the EEG data separated ANOVAs were carried out for each EEG band
including, again, the factor Age (three levels: Children vs. Young vs. Middle-aged)
and four within-subjects factors: Task (three levels: Orthographic vs. Phonolog-
ical vs. Semantic), Interval (two levels: Baseline vs. Word processing), Region
(two levels: Anterior vs. Posterior) and Laterality (two levels: Left vs. Right
hemisphere).
Post-hoc comparisons were performed using the Tukey HSD test (p < 0.05), and
the Greenhouse–Geisser correction was applied when necessary, that is when vari-
ables with more than two levels were involved.
3
For each EEG band, we indicated the typical frequency range and the “effective
range”, that is the real width of each EEG band.
 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
Table 1
Behavioral analysis computed on response times (RTs, in milliseconds) and error rates (ERs) for each age group.
Analysis Response times (RTs, in ms)
Task Orth. Phon.
Children 1497.19 (SD: 424.3) 1530.25 (SD: 401.5)
Young 750.34 (SD: 183.5) 798.12 (SD: 165.2)
Middle-aged 874.38 (SD: 228.9) 1021.38 (SD: 300.6)
Orth., Orthographic task; Phon., Phonological task; Sem., Semantic task.
3. Results
3.1. Behavioral results
In order to control for confounding factors, we carried
out separate ANOVAs for Gender, Handedness and Educa-
tion level. Groups showed no differences in sex distribu-
tion (F(2,67) = 0.63, p = 0.53) or percentage of right-handedness
(F(2,67) = 1.31, p = 0.27). As expected, the two-way Age by Edu-
cation interaction (F(2,67) = 130.60, p < 0.001) revealed the greater
education level in both adult groups (13 and 11.7 years for Young
and Middle-aged participants, respectively) compared with Chil-
dren (4.5 years; p < 0.001; Cohen’s d = 8.68 and 2.96, both very large
effects).
Direct Digit Span (DS) performance was also expected to
vary across groups. Interestingly, the Age variable (F(2,67) = 12.94,
p < 0.001) showed greater DS in young adults (7.00) than in either
children (5.43; p < 0.001; Cohen’s d = 1.33, very large effect) or
middle-aged participants (5.95; p < 0.01; Cohen’s d = 0.93, large
effect).
Performance analyses showed slower RTs in children (mean:
1690 ms) than in the two adult groups (p < 0.001; means: 839
and 1006 ms, Cohen’s d = 2.15 and 1.65, both very large effects,
for young and middle-aged participants, respectively: Age main
effect: F(2,67) = 58.34, p < 0.001). Moreover and regardless of age
group, RTs on the Semantic task (1377 ms) were longer than
those on the Phonological one (1116 ms; Cohen’s d = 0.54, medium
effect) which, in turn, were longer than RTs on the Orthographic
task (1041 ms; Cohen’s d = 0.15, small effect; Task main effect:
F(2,134) = 85.40, p < 0.001, GG ε = 0.93). The significant two-way
Age by Task interaction (F(4,134) = 14.02, p < 0.001, GG ε = 0.93)
revealed that, independent of task, children were slower when
compared with both adult groups (all p < 0.001; all Cohen’s d ≥ 1.45,
resulting in very large effects; Table 1). But, in turn, the middle-
aged group showed slower RTs than young participants on both
Phonological (p < 0.001; Cohen’s d = 0.93, large effect) and Seman-
tic tasks (p < 0.05; Cohen’s d = 0.71, medium effect), whereas they
did not differ during the Orthographic task (Table 1). With regard
to within-group differences, children’s RTs were slower during
Semantic than either Phonological or Orthographic tasks (p < 0.001;
Cohen’s d = 1.17 and 1.21, both very large effects), whereas young
adults exhibited slower RTs for the Semantic with respect to the
Orthographic task (p < 0.01; Cohen’s d = 1.15, very large effect).
ER analysis showed both Age (F(2,67) = 18.19, p < 0.001) and Task
(F(2,134) = 40.26, p < 0.001, GG ε = 0.98) main effects. Children made
more errors (6.9%) as compared to young adults (2.9%, p < 0.001;
Cohen’s d = 0.92, large effect) and middle-aged participants (3.6%,
p < 0.001; Cohen’s d = 0.77, large effect). Concerning the main effect
of task, the Semantic processing revealed higher ERs compared
with the other two tasks (all p < 0.001; Cohen’s d = 1.19 and 0.61,
very large and medium effect, for Phonological and Semantic tasks,
respectively). In addition, the Orthographic task displayed more
errors than did the Phonological one (p < 0.01; Cohen’s d = 0.49,
medium effect). The significant two-way Age by Task interac-
tion (F(4,134) = 9.16, p < 0.001, GG ε = 0.98) revealed that children
made more errors compared with the two adult groups during
261
Error rates (ERs)
Sem. Orth. Phon. Sem.
2041.91 (SD: 471.6) 6.74% (SD: 4.89) 3.13% (SD: 2.53) 10.89% (SD: 4.46)
968.85 (SD: 196.3) 2.67% (SD: 3.64) 1.36% (SD: 1.33) 4.66% (SD: 3.07)
1121.94 (SD: 236.2) 2.94% (SD: 2.34) 3.25% (SD: 3.54) 4.56% (SD: 2.00)
both Orthographic and Semantic tasks (all p < 0.001; all Cohen’s
d ≥ 0.93, resulting in large effects), but not during the Phonolog-
ical task (Table 1). Adult groups did not differ in ERs. With regard
to within-group differences, children’s ERs were greater during
Semantic and Orthographic tasks (all p < 0.001; Cohen’s d = 2.14 and
0.93, very large effects) compared with phonological processing,
whereas only young adults exhibited greater ERs on the Seman-
tic vs. the Phonological task (p < 0.01; Cohen’s d = 1.39, very large
effect; Table 1).
3.2. FFT spectral analysis results
Fig. 1 shows an overall view of all normalized EEG bands
(0.5–100 Hz) in the three age groups. Low frequency rhythms –
i.e., delta, theta and alpha bands – decreased with increasing age,
whereas high frequency rhythms – i.e., beta and gamma bands –
showed the reversed pattern, with increasing amplitude across age.
Indeed, low frequency bands had larger weight in children, their
percentage making up about 50% of the whole EEG spectrum (Fig. 1,
left column), whereas high frequency bands had a strong influ-
ence in both adult samples, particularly in the middle-aged group
in which the overall percentage exceeded 70% of the whole EEG
spectrum (Fig. 1, right column).
3.3. Delta band analysis
Overall, ANOVA carried out on the normalized ␦ band ampli-
tude showed a significant main effect of the between-subjects
factor Age (F(2,67) = 93.74, p < 0.001): children exhibited greater
␦ amplitude (i.e., 17.75%) than both adult groups (all p < 0.001;
Cohen’s d ≥ 1.77, resulting in very large effects), and young adults,
in turn, had greater ␦ levels than middle-aged participants (i.e.,
12.32% and 8.25%, respectively; p < 0.001; Cohen’s d = 1.32, very
large effect). In addition, regardless of age group, higher ␦ ampli-
tude was reached in the word processing (13.23%) compared with
the baseline interval (12.31%; Interval main effect: F(1,67) = 175.22,
p < 0.001; Cohen’s d = 0.18, small effect). Delta amplitude was
greater on posterior (13.71%) than anterior sites (11.83%; region
main effect: F(1,67) = 46.80, p < 0.001; Cohen’s d = 0.38, small effect)
and within the right rather than the left hemisphere (12.90%
vs. 12.64%; Laterality main effect: F(1,67) = 4.05, p < 0.05; Cohen’s
d = 0.04, negligible effect). However, the two-way Age by Laterality
interaction (F(2,67) = 11.80, p < 0.001) revealed specific patterns of
␦ band (Fig. 2, first row). Groups exhibited decreasing ␦ amplitude
with increasing age, but children and adults also exhibited different
patterns of lateralization. Indeed, children and middle-aged partici-
pants showed bilateral ␦ distribution, whereas higher ␦ levels were
found in right vs. left hemisphere of young adults (p < 0.01).
3.4. Theta band analysis
ANOVA carried out on the normalized ϑ rhythm showed
a significant main effect of the between-subjects factor Age
(F(2,67) = 30.76, p < 0.001): children exhibited greater ϑ ampli-
tude (11.66%) than both young adult and middle-aged participants
(8.29% vs. 6.87%, respectively; p < 0.001; Cohen’s d ≥ 0.58, resulting
262 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
Fig. 2. Spline maps of normalized delta (␦, first row), alpha (␣, second row) and high-beta (␤2, last row) EEG bands, expressed as percentage of spectral contribution with
respect to 0.98–100 Hz range in children, young adults and middle-aged participants for Orthographic (Orth.), Phonological (Phon.) and Semantic (Sem.) tasks.
in medium effects). Like in the ␦ band analysis and independent
of the age group, the ϑ amplitude was greater in posterior (9.94%)
than in anterior sites (7.94%; Region main effect: F(1,67) = 101.13,
p < 0.001; Cohen’s d = 0.62, medium effect). In addition, the four-
way Age by Task by Region by Laterality interaction (F(4,134) = 3.34,
p < 0.01, GG ε = 0.96) revealed specific, task-dependent patterns of
ϑ lateralization in each group (Fig. 3). Overall, children showed
greater ϑ amplitude than did both adult groups, regardless of
Fig. 3. Theta (ϑ) EEG band: significant four-way Age by Task by Region by Lateral-
ity interaction. Mean ϑ amplitude is depicted for children (white squares), young
adults (gray triangles) and middle-aged participants (black circles). LH = left hemi-
sphere; RH = right hemisphere. Asterisks indicate significant between hemisphere
differences (Tukey HSD, *p < 0.05).
cortical regions, in line with the already mentioned Age main
effect.
Concerning laterality patterns, children had bilateral ϑ distribu-
tion during the Orthographic task and posterior left-lateralized ϑ
activity during both linguistic tasks (i.e., the Phonological and the
Semantic ones; all p < 0.001, Fig. 3b). During all tasks, young adults
exhibited significant right-lateralized ϑ amplitude in anterior (with
the exception of the Semantic one; all p < 0.001, Fig. 3a) and pos-
terior regions (Orthographic and Phonological: p < 0.05, Semantic:
p < 0.001, Fig. 3b). Middle-aged participants revealed larger right
than left ϑ amplitude in anterior sites in both Orthographic and
Semantic tasks (all p < 0.001, Fig. 3a), but bilateral ϑ activity in the
Phonological one as well as over posterior sites in all tasks (Fig. 3b).
3.5. Alpha band analysis
ANOVA carried out on the normalized ␣ band showed signifi-
cant main effects in all within-subjects factors. Thus, independent
of Age, the Semantic task revealed greater ␣ amplitude than the
Orthographic one (10.33% vs. 10.05%, respectively; p < 0.05; Cohen’s
d = 0.07, negligible effect), whereas no differences were found for
the Phonological one (10.24%; Task main effect: F(2,134) = 3.88,
p < 0.05, GG ε = 0.99). The word processing interval displayed lower
␣ amplitude (10.06%) with respect to the baseline (10.35%; Interval
main effect: F(1,67) = 21.63, p < 0.001; Cohen’s d = 0.08, negligible
effect), and the posterior regions had higher ␣ amplitude than the
anterior ones (12.05% vs. 8.36%, respectively; Region main effect:
F(1,67) = 262.78, p < 0.001; Cohen’s d = 1.25, very large effect). Sig-
nificant overall greater ␣ amplitude was found in right vs. left
hemisphere (10.35% vs. 10.06%, respectively; Laterality main effect:
F(1,67) = 6.49, p < 0.01; Cohen’s d = 0.07, negligible effect). Similarly
to ϑ band results, the four-way Age by Task by Region by Laterality
interaction (F(4,134) = 3.42, p < 0.01, GG ε = 0.98) revealed specific
task-dependent patterns of ␣ lateralization in each group (Fig. 2,
second row).
Unlike ␦ and ϑ rhythms, ␣ amplitude was higher in children than
in both adult groups only in anterior sites (all p < 0.001) and young
adults, in turn, had greater ␣ amplitude than middle-aged partic-
ipants (all p < 0.001; Fig. 4a). Instead, in posterior locations, young
adults showed greater ␣ levels than children and middle-aged
participants, particularly during Phonological and Semantic tasks
(all p < 0.001 for left and right hemisphere, respectively; Fig. 4b).
Children had higher ␣ amplitude than middle-aged participants
over both posterior sites during the Orthographic task, but they
 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
Fig. 4. Alpha (␣) EEG band: significant four-way Age by Task by Region by Lateral-
ity interaction. Mean ␣ amplitude is depicted for children (white squares), young
adults (gray triangles) and middle-aged participants (black circles). LH = left hemi-
sphere; RH = right hemisphere. Asterisks indicate significant between hemisphere
differences (Tukey HSD, *p < 0.05).
showed higher ␣ in left posterior locations during phonological
and semantic processing (all p < 0.001; Fig. 4b). Concerning lat-
erality patterns, children had bilateral ␣ distribution during the
Orthographic task and posterior left-lateralized ␣ amplitude dur-
ing both linguistic tasks (i.e., the Phonological (p < 0.01) and the
Semantic ones (p < 0.001), Fig. 4b), a result similar to that of the
ϑ band analysis. Young adults, meanwhile, exhibited significant
right-lateralized ␣ amplitude in anterior and posterior regions
during the Phonological task (all p < 0.01, Fig. 4), and showed ante-
rior right-lateralization during the visuo-perceptual processing
(i.e., the Orthographic task; p < 0.001, Fig. 4a) and posterior right-
lateralization during the semantic processing (p < 0.001, Fig. 4b).
By way of contrast, middle-aged participants revealed anterior ␣
right-lateralization (Orthographic and Semantic tasks: p < 0.001,
Phonological task: p < 0.01, Fig. 4a) and posterior bilateral distri-
bution in all tasks.
3.6. Low-beta (ˇ1) band analysis
ANOVA carried out on the normalized ␤1 band showed sig-
nificant effects in all within-subjects factors, revealing patterns
of activation similar to the ␣ band analysis, namely greater ␤1
amplitude was found during the Semantic (11.66%) and the Phono-
logical (11.59%) vs. the Orthographic task (11.40%; p < 0.001 and
p < 0.01, respectively; Task main effect: F(2,134) = 80174, p < 0.001,
GG ε = 0.94; Cohen’s d ≥ 0.11, resulting in negligible effects). The
baseline interval revealed higher ␤1 amplitude than the word pro-
cessing one (11.71% vs. 11.39%, respectively; Interval main effect:
F(1,67) = 82.17, p < 0.001; Cohen’s d = 0.14, negligible effect). Poste-
rior regions had higher ␤1 activity than anterior ones (12.31% vs.
263
Fig. 5. Low-beta (␤1) EEG band: significant four-way Age by Task by Region by Later-
ality interaction. Mean ␤1 amplitude is depicted for children (white squares), young
adults (gray triangles) and middle-aged participants (black circles). LH = left hemi-
sphere; RH = right hemisphere. Asterisks indicate significant between hemisphere
differences (Tukey HSD, *p < 0.05).
10.79%, respectively; Region main effect: F(1,67) = 83.05, p < 0.001;
Cohen’s d = 0.62, medium effect), and significantly greater ␤1
amplitude was found in right vs. left hemisphere (11.65% vs. 11.45%,
respectively; Laterality main effect: F(1,67) = 6.44, p < 0.01; Cohen’s
d = 0.08, negligible effect). Likewise in ϑ and ␣ band analyses, the
four-way Age by Task by Region by Laterality interaction was sig-
nificant (F(4,134) = 3.62, p < 0.01, GG ε = 0.96; Fig. 5).
Similar to the ␣ band pattern, the ␤1 amplitude was higher
in children than in both adult groups only over anterior sites (all
p < 0.001) but, unlike the ␣ band, middle-aged participants had
greater ␤1 levels with respect to young adults (all p < 0.001, Fig. 5a).
In posterior locations, the middle-aged group showed greater ␤1
levels as compared to young adult participants (all p < 0.001),
which, in turn, exhibited higher ␤1 amplitude than did children
(all p < 0.001, with the exception of left locations for the seman-
tic processing, in correspondence with which no group differences
were found; Fig. 5b). Concerning the hemispheric lateralization
across tasks, groups revealed a pattern very similar to that found
for the ␣ band analysis. Thus, children had bilateral ␤1 distribu-
tion during the Orthographic task and posterior left-lateralized
␤1 amplitude during both linguistic tasks (i.e., the Phonological
(p < 0.01) and the Semantic ones (p < 0.001), Fig. 5b). The young
adult sample exhibited significant right vs. left ␤1 amplitude in
anterior regions during both Orthographic and Phonological tasks
(all p < 0.001, Fig. 5a) and in posterior regions during the Seman-
tic one (p < 0.05, Fig. 5b). Middle-aged participants showed greater
right vs. left anterior ␤1 amplitude (p < 0.001 during Orthographic
and Semantic tasks, p < 0.05 during the Phonological one, Fig. 5a)
and posterior bilateral ␤1 distribution in all tasks (Fig. 5b).
264 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
Fig. 6. High-beta (␤2) EEG band: significant four-way Task by Interval by Region
by Laterality interaction. Mean ␤2 amplitude reached by all groups collapsed is
depicted for Orthographic (gray squares on gray lines), Phonological (white cir-
cles on thick black lines) and Semantic tasks (white diamonds on thin black lines).
LH = left hemisphere; RH = right hemisphere. Asterisks indicate significant between
hemisphere differences (Tukey HSD, *p < 0.05).
3.7. High-beta (ˇ2) band analysis
Overall, ANOVA carried out on the normalized ␤2 band
showed a significant main effect of the between-subjects factor
Age (F(2,67) = 7.25, p < 0.001): middle-aged participants exhibited
greater ␤2 amplitude than did children (i.e., 9.61% vs. 8.43%, respec-
tively; p < 0.001; Cohen’s d = 0.82, large effect), but no differences
were found in the young adult group (8.83%). In addition, regard-
less of age group, the highest ␤2 amplitude was reached in linguistic
(i.e., Phonological, 8.98%, and Semantic, 9.02%, tasks) with respect
to non-linguistic processing (i.e., the visuo-perceptual, Ortho-
graphic task, 8.87%; p < 0.05 and p < 0.01, respectively; Task main
effect: F(2,134) = 5.05, p < 0.01, GG ε = 0.99; Cohen’s d ≥ 0.11, result-
ing in negligible effects). Concerning the temporal dimension, the
word processing interval revealed lower ␤2 amplitude (8.86%) with
respect to the baseline (9.05%; Interval main effect: F(1,67) = 62.48,
p < 0.001; Cohen’s d = 0.13, negligible effect). In addition, unlike all
other EEG bands, ␤2 amplitude was greater on anterior (9.41%) than
posterior sites (8.50%; Region main effect: F(1,67) = 65.55, p < 0.001;
Cohen’s d = 0.73, medium effect). Unlike the other EEG bands so
far analyzed, no interaction including the group factor was found
for the ␤2 band ANOVA. However, the four-way Task by Interval
by Region by Laterality interaction was significant (F(2,134) = 4.21,
p < 0.05, GG ε = 0.99), revealing a specific task-dependent pattern of
lateralization, regardless of age group (Fig. 2, last row).
On anterior locations (Fig. 6a), significantly greater ␤2 ampli-
tude was found in left vs. right hemisphere in both intervals during
Phonological and Semantic tasks (all p < 0.001). Conversely, the
non-linguistic task, i.e., the Orthographic one, exhibited bilateral
␤2 distribution (Fig. 6a). In addition, both Phonological and Seman-
tic tasks showed greater left ␤2 amplitude in comparison with
the Orthographic one (baseline: p < 0.05 and p < 0.001, respectively;
word processing interval: all p < 0.001), whereas only the Semantic
task displayed significant greater ␤2 amplitude in right sites (all
p < 0.001; Fig. 6a). Over posterior locations (Fig. 6b) the Semantic
task exhibited greater left ␤2 amplitude in the baseline interval
(p < 0.01), but the other two tasks were characterized by bilateral
␤2 distribution, regardless of intervals. In addition, during the base-
line interval, the ␤2 amplitude was higher in left locations during
the Phonological and the Semantic with respect to the Orthographic
task (p < 0.01 and p < 0.001, respectively), and in both hemispheres
(left: p < 0.01; right: p < 0.001) during the word processing interval.
4. Discussion
The present study aimed at demonstrating that age-related
skilled reading, achieved from continuous interaction with written
word, plays a role in the development of the typical left lateral-
ization of linguistic networks. Based on our previously validated
paradigm (Penolazzi et al., 2008; Spironelli and Angrilli, 2006,
2009b; Spironelli et al., 2006, 2008), this experiment compared
three different age groups in order to investigate the functional lin-
guistic role of low and high frequency bands across age within the
linguistic framework, by using the same experimental paradigm
and tasks.
Overall, children’s longer RTs (compared with adult groups)
suggest that our 10-year-old participants have not completely
reached the full development of their linguistic skills – at least
for the reading process – although their reading speed, measured
using several standardized tests, fell into the range proper for
their age (Spironelli et al., 2010). However, children’s performance
shows, on average, low levels of error rates, particularly for the
Phonological task: in line with this, no group differences were
found. Concerning the Digit Span test, indexing the verbal work-
ing memory, children achieved lower DS scores, probably because
of their incomplete cognitive and cerebral development, whereas
middle-aged participants’ low span may represent an initial, par-
tial process of deterioration of the verbal, short-term memory. This
was further supported by their longer RTs to linguistic tasks (i.e.,
the Phonological and Semantic ones) as compared with those of
young adults, whereas no difference between adult groups was
found for the Orthographic, non-linguistic task. Yet, despite this
decay of important components of language processing, middle-
aged participants achieved good linguistic performance (i.e., low
error rates), when compared with the young adult group, probably
because of their long-term linguistic experience which allowed to
develop highly interconnected, automated and functional linguistic
networks within the left hemisphere.
With regard to electrophysiological data, the qualitative analysis
of the whole normalized EEG spectrum attested that the typical pat-
tern found in children (i.e., increased amplitude of low frequency
and decreased amplitude of high frequency rhythms) gradually
tends to reverse over age: beta and gamma bands being prevalent in
middle-aged participants. Concerning this point, ANOVA analyses
carried out separately for each EEG band confirmed the significant
Age main effect in delta, theta as well as high-beta (␤2) frequency
rhythms, low frequency bands being more prevalent in children
than in both adult groups and high frequency rhythms being more
dominant in middle-aged participants than in children. One addi-
tional important result was found in the delta band analysis which
revealed, in children, bilateral delta distribution, regardless of task.
In young adults, by contrast, greater delta amplitude over right than
left cortical sites was found, a result indicating a relative inhibi-
tion of right with respect to left hemisphere. This finding suggests
 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
not only that anterior regions are not yet completely developed in
children aged 10, but also that, in linguistic networks, there is a
significant maturation lag (in terms of lateralization) of left frontal
regions. Indeed, past studies carried out in neurological patients
suffering from tumors or cerebrovascular accidents have stated that
the delta rhythm is a steady marker of neuronal damage (e.g., De
Jongh et al., 2001; Tanaka et al., 1998; Vieth et al., 2001), but more
recent evidence further clarified this band as a marker of functional
deficit of high level cognitive processes in dyslexic, aphasic as well
as schizophrenia patients (e.g., Hensel et al., 2004; Penolazzi et
al., 2008; Spironelli and Angrilli, 2009b; Spironelli et al., in press).
With regard to this approach, the present study investigated the
developmental aspects of delta functional meaning and showed, in
children, a clear-cut lack of the typical adult linguistic hemispheric
specialization, a result which demonstrates the long-term difficult
and effortful development of reading.
Analyses of theta and alpha EEG bands allowed us to draw simi-
lar conclusions. Indeed, children showed greater theta and alpha
amplitudes compared to adults, particularly over anterior loca-
tions. However, unlike the delta rhythm, theta and alpha bands
also revealed task-dependent patterns of lateralization in every age
group. Thus, children exhibited significantly greater left vs. right
theta and alpha amplitude over posterior sites in those tasks which
required linguistic processing (i.e., the Phonological and the Seman-
tic one; Figs. 3b and 4b), whereas bilateral distribution of theta and
alpha rhythms was shown over anterior locations (Figs. 3a and 4a)
and for the Orthographic task in all analyzed sites (Figs. 3 and 4).
Conversely, adult groups revealed more specific, task-dependent
patterns of lateralization. In detail, young adults had significantly
greater right vs. left theta amplitude, in both anterior and posterior
sites, during the visuo-perceptual and the phonological process-
ing, but in the semantic judgment the same pattern was found
in posterior locations. The alpha rhythm revealed even greater
right hemispheric specialization, with young adults showing larger
right-lateralization in anterior regions during the visuo-perceptual
processing, in posterior sites during the semantic judgment, and
in both anterior and posterior sites during the Phonological task
(Fig. 4). Middle-aged participants showed similar patterns of theta
band lateralization for Orthographic and Semantic tasks (signifi-
cantly greater right vs. left amplitude in anterior locations) and
bilateral distribution for the Phonological one, whereas no task
effect was found in the alpha rhythm (greater anterior right vs.
left amplitude, regardless of task; Fig. 4). Taken together, these
results suggest that, in a linguistic context, low frequency bands
have different functional roles according to age and maturity. In
agreement with the past literature on language, the functional
interpretation of theta and alpha rhythms in children points to a
not completely automated learning mechanism underlying reading
skills (Caplan and Glaholt, 2007), which seems to be related to the
working memory involvement (Bastiaansen et al., 2002; Klimesch,
1999; Scheeringa et al., 2009). Indeed, the significant left posterior
lateralization of theta as well as alpha bands during Phonological
and Semantic tasks suggests that left posterior regions are selec-
tively involved in the early processing of linguistic information,
such as grapheme-phoneme conversion and storage and retrieval
of phonological information (Burton et al., 2000). On the other hand,
the observed greater theta/alpha amplitude in left posterior sites
could indicate a difficult, not yet complete, integration and hierar-
chy of left anterior and posterior linguistic centers necessary for the
full development of the phonological awareness and the achieve-
ment of efficient reading skills. In adult groups, theta and alpha
rhythms showed task-dependent modulations with greater right
vs. left hemisphere amplitudes: these patterns suggest that, when
the linguistic network is completely developed and interconnected
within the left hemisphere, the functionally less efficient linguistic
regions of the right hemisphere are relatively inhibited (Spironelli
265
and Angrilli, 2006). In a recent study in which alpha and theta EEG
power were measured together with fMRI during a working mem-
ory maintenance task, Scheeringa et al. (2009) found significant
correlations between the increase of frontal theta power and the
decrease of BOLD signals, and between the posterior right alpha
increase and the decrease of BOLD signals in the primary visual
cortex and the posterior part of the middle temporal gyrus dur-
ing the maintenance interval. Authors concluded that an increase
in alpha power represents the cortical marker of top-down func-
tional inhibition of those regions not involved in the maintenance of
the relevant information in the working memory. Thus, in line with
Klimesch et al. (2007) and Scheeringa et al. (2009), an active inhibi-
tion mechanism acts on right anterior, posterior or both locations of
language homologues, according to the specific linguistic process-
ing required by the task. This cognitive skill is equally efficient in
both young adults and middle-aged participants, regardless of the
initial deterioration of the verbal working memory in middle-aged
participants.
Concerning the statistical analyses of high frequency bands, typ-
ically regarded as markers of cognitive processing, integration and
learning (e.g., Jensen et al., 2007; Miltner et al., 1999; Steriade,
2000; Tallon-Baudry and Bertrand, 1999; Weiss and Rappelsberger,
1998), we found evidence that only the high-beta (␤2) rhythm,
ranging from 21 to 28 Hz, revealed a significant pattern of linguis-
tic activation in agreement with the functional meaning provided
by the past literature. Instead, the low-beta (␤1) rhythm, ranging
from 13 to 20 Hz, showed a distribution similar to that exhibited
by slower EEG bands, regardless of age group. In our opinion, this
result suggests that, in the linguistic domain, the low-beta rhythm
represents a transition from slow to fast rhythms, rather than a
clear-cut rhythm with a specific functional meaning. From this per-
spective, similarly to theta and alpha bands, the low-beta band
could characterize, in adults, the active inhibition mechanism over
contralateral regions not involved in the main left linguistic net-
works (Klimesch et al., 2007). The high-beta (␤2) band showed
significantly greater activation of left vs. right anterior sites in all
groups (indeed, Fig. 6 shows the results with age group collapsed,
since the five-way interaction – including Age-group variable –
was not significant). In detail, this pattern of left lateralization
marked both Phonological and Semantic tasks – i.e., those which
required specific linguistic processing – whereas ␤2 amplitude was
bilaterally distributed during the Orthographic task – i.e., when a
non-linguistic, visuo-perceptual matching was requested (Fig. 2,
last row). Thus, in agreement with past studies on language local-
ization (e.g., Bookheimer, 2002; Hagoort, 2005; Poldrack et al.,
1999; Xiang et al., 2010), the high-beta band marks the typical
left hemisphere specialization for language in adult samples, but
the novel finding with respect to the past literature is the discov-
ery that this band can also reflect language dominance in children
with incomplete maturation of linguistic reading networks. The
only difference between phonological and semantic processes was
found in the baseline, an interval in which, given the blocked
presentation, a task-dependent pre-activation may occur in lin-
guistic networks: the Semantic task showed greater activation of
left vs. right posterior regions (Fig. 6b). This finding suggests that
the high-beta rhythm can roughly differentiate the tasks before
stimulus-driven linguistic processes develop. At the same time, this
band reflects the integration of the crucial features of each linguistic
task (i.e., phonological information for rhyming task, and category
classification for semantic judgment) when the linguistic process
takes place. Notwithstanding slow rhythm analyses in children and
adults showed inverted patterns of lateralization (Fig. 2, first and
second rows), pointing to different levels of linguistic development
and automation, the lack of age-group lateralization differences for
␤2 band suggests that this band can reflect the few specialized lin-
guistic networks active in children’s left hemisphere (Fig. 2, last
266 C. Spironelli, A. Angrilli / Biological Psychology 85 (2010) 258–267
row), and therefore represents the best EEG marker for investigat-
ing left hemisphere linguistic dominance, making it applicable to
both children and adult samples. The only study in the past litera-
ture which has focused on the developmental aspects of language
lateralization using the CNV paradigm in a rhyming task (Grossi et
al., 2001) found that the linguistic left lateralization of the Contin-
gent Negative Variation (CNV) started at 10–11 years and increased
linearly with age until 19–20 years. The CNV wave reflects the acti-
vation of a large population of cortical neurons, but is less sensitive
to the activity of a more limited amount of neurons embedded in
linguistic networks. Therefore, the lack of left linguistic lateraliza-
tion found at the age of 10 by Grossi et al. (2001) for the CNV is
related to an overall reduced lateralization and expertise in chil-
dren. From the present study, the beta EEG band appears to be more
sensitive to the reduced, yet present, left lateralization in children.
Thus, to our knowledge, this is the first investigation showing the
capability of an electrophysiological marker to measure a consis-
tent, left hemisphere dominance during written word reading tasks
in children aged 10. In addition to this result, it can be noted that
the Age main effect showed significantly lower ␤2 amplitude in
children than in middle-aged participants, a result which suggests
that linguistic cortical centers in children’s frontal lobes are not yet
complete–an observation in agreement with the well-known delay
in maturation and myelinization of frontal lobes which is complete
at the age of about 18. This could be the reason why, during Phono-
logical and Semantic tasks, school readers needed additional time,
probably because of the limited capacity of the verbal working
memory and the relative immaturity of left posterior regions (as
indexed by theta and alpha activity). Therefore, the high-beta band
was sensitive to the functional integration of essential informa-
tion provided by different systems (and different EEG frequencies)
when the linguistic cortical areas are still not completely devel-
oped. According to von Stein and Sarnthein (2000), in adults this
anterior language center (in the left inferior frontal gyrus) plays
an important role in unification processes (Hagoort, 2005; Xiang et
al., 2010), is able to organize not only linguistic functions, but also
hierarchically structured behaviors (Koechlin and Jubault, 2006),
and acts through an active inhibition process over the right homo-
logues not involved in that specific task (as indexed by slow EEG
bands).
In conclusion, EEG spectral analysis was effective at measuring
functional and developmental aspects of language. The EEG delta
band, regardless of language, is an unambiguous index of gener-
alized inhibitory process both in adults and in children: indeed,
this is a very slow rhythm and neurons synchronized in this fre-
quency are damaged, disconnected (e.g., Spironelli and Angrilli,
2009; Spironelli et al., in press) or not engaged in specific cognitive
processes. In children delta EEG is higher than in adults because of
incomplete cortical maturation, and is typically even larger in chil-
dren with learning disabilities (e.g., in dyslexic children; Penolazzi
et al., 2008). Concerning other slow bands, alpha and theta EEG
frequency bands have opposite functional roles in adults and chil-
dren, at least within the linguistic framework. In adults, in whom
language is fully automated, the key role of anterior left regions
becomes clear-cut in the range of high-beta frequencies. At the
same time, an active process of inhibition of task-irrelevant corti-
cal regions within the right hemisphere is shown by slow rhythms,
according to Klimesch et al. (2007). It is important to underline that
the two adult groups showed almost no differences in their patterns
of activation, suggesting that there is no effect of moderate aging on
the specialization and the functioning of linguistic networks, which
are resistant to the observed initial, partial process of deterioration
of the verbal working memory. Conversely, in children, in whom
linguistic automation is not yet complete, slow and fast rhythm
patterns suggest that different mechanisms are critically involved
in both phonological and semantic processing—i.e., there is a signif-
icant increase of left posterior activation (theta and alpha bands),
possibly associated with the early processing of linguistic informa-
tion, its transfer in working memory (Burton et al., 2000; Klimesch,
1999; Scheeringa et al., 2009) and the concurrent activation of spe-
cific high level networks in left anterior regions (high-beta band),
involved in the integration of task-dependent linguistic informa-
tion (von Stein and Sarnthein, 2000). The high-beta band was, in
the present linguistic paradigm, the only rhythm which showed
the same coherent left hemispheric pattern across all age groups,
including children not yet fully competent in reading, with greater
amplitude to linguistic tasks (i.e., the Phonological and the Seman-
tic ones) in left frontal clusters, a result in agreement with current
theories on the central role of left Broca area in the organization
and integration of the whole language (Bookheimer, 2002; Hagoort,
2005).
Acknowledgements
This study was supported by a grant (PRIN 2006110284 001)
from the MIUR (Ministero dell’Istruzione, dell’Università e della
Ricerca) and University of Padova project n. CPDA047438 to A.A.
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