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2014 27th SIBGRAPI Conference on Graphics, Patterns and Images

Brain Mapping and Interpretation of Reading Processing in Children Using


EEG and Multivariate Statistical Analysis

Fabio Theoto Rocha and Carlos Eduardo Thomaz


Department of Electrical Engineering, FEI, Sao Paulo, Brazil
Armando Freitas da Rocha
Research in Articial and Natural Intelligence, Sao Paulo, Brazil
Eduardo Massad
Department of Medical Informatics, FMUSP, Sao Paulo, Brazil

Abstract temporal connections and is described as the lexical route,


the other involves parieto-frontal connections and is de-
Difculties in learning to read may have a number of scribed as the phonological route [5, 7, 6], being the distur-
causes and children tend to experience on the phonolog- bance of each of these routes named as surface and phono-
ical route the most common disturbance in this cognitive logical dyslexia respectively [23, 37, 53]. In other words,
task. Using two sample groups of children with and with- the rst route translates the visual information transmitted
out reading difculties and their corresponding EEG sig- by the string of letters of each word, processed by tempo-
nals captured during the reading processing, we describe in ral neurons grouped in the previous identied word-form
this work a set of techniques that investigates such distur- area directly in its meaning through the area of Wernicke,
bance by generating whole brain mappings based on the en- named from a neurologist. Neurons from this area estab-
tropy of each EEG electrode and non-supervised and super- lish the connection from the string of letters of each word to
vised multivariate statistical analyses. Our experimental re- multiple brain regions depending on the word meaning and
sults have clearly showed specic neural organizations well semantic eld. The second route converts each grapheme or
suited to interpreting the word/phrase reading processing in group of grapheme (syllable), identied by parietal neurons,
these children. We believe that these techniques might be- to the sound it represents, what is operated by frontal neu-
come an effective computational tool in helping the diag- rons, to construct the sound of the word and nally access
nostic process of children with learning disabilities. its meaning, again through Wernickes area. Children may
experiment one or both of these routes disturbance, but what
is more frequent to observe is the difculty children expe-
rience in the grapheme-phoneme conversation involved on
1. Introduction the phonological route.
In this context, this work uses the Distributed Intelligent
Difculties in learning to read may have a biological Processing System (DIPS) model [48, 11, 9] to process the
cause, the neural connections may not organize themselves EEG signal aiming to summarize the information provided
accordingly during the neurological development since the by each electrode from the conventional 10/20 system [32]
fetal stage till the rst childhood due to both genetic [52, and analyse the reading processing in children. DIPS was
1, 35, 42, 17, 51, 38, 43, 15, 19] and environmental fac- rst developed on the eld of Articial Intelligence in order
tors, such as malnutrition [39, 21, 41], preterm birth [31], to formalize systems composed of multiple agents, where
mother depression [21], stress suffered by the mother dur- each one of these agents could specialize itself in the pro-
ing pregnancy [24, 41], use of drugs [41, 51, 8], among oth- cessing of some specic kind of information and could par-
ers. ticipate on various different associations with other agents
These factors may disrupt one or both of the principal to solve complex tasks [4, 12, 36, 45, 46, 55].
neural circuits appointed nowadays as underlying human More specically, assuming that the brain can be under-
reading ability according to the dual-route model [5, 7, 23, stood as a DIPS model and based on the neural efciency
37, 6, 53]. Figure 1 illustrates the brain areas involved on the theory [22], we describe and implement here a technique of
dual-route model of reading. One circuit involves occipto- brain mapping that has been used to investigate the associ-

1530-1834/14 $31.00 2014 IEEE 251


DOI 10.1109/SIBGRAPI.2014.19
DL group particularly exhibited statistical signicant occur-
rences such as motherly high stress index during pregnancy,
use of tobacco and alcohol, low birth weight, among others,
suggesting the aforementioned difculties in reading by this
group due to possibly neurological disturbances.
Both DL and CO sample groups have been composed of
10 children (5 boys, 5 girls). The age of the DL children has
varied from 10 to 14 and of the CO children from 8 to 12.
This age difference occurred owing to the school gap of DL
children. Both groups had to solve a 6-word or -phrase read-
ing task where they have to select an image (clicking on it)
out of ve that best describes the corresponding meaning of
the word or phrase presented as written language above the
image options. Figure 2 shows an example of a word read-
Figure 1. Brain areas involved on the dual-
ing task carried out in the experiments.
route model of reading.
To demand from children an equivalent cognitive effort,
the word or phrase reading task has been selected according
to each child development - those who could read words
ations among the agents of the neural system during cog- without any error did the phrase task, whereas those who
nitive tasks, illustrating these associations by means of a could not read phrases did the word one.
non-supervised multivariate statistical technique [16, 48].
Additionally, as a new contribution, we extend in this arti- 3. Methods
cle the use of this methodology to investigate the efciency
of a supervised multivariate statistical technique in discrim- Children solved tasks while their EEG signals were reg-
inating between the neural organization of a normal read- istered using 20 electrodes placed according to the 10/20
ing group and a group having learning difculties possibly system [32], as illustrated in Figure 3. Statistical analysis of
caused by neuronal disorder such as dyslexia. Our exper- their performance and the recorded EEG signals provided
imental results have showed specic neural organizations the data to investigate the aforementioned cognitive func-
well suited to interpreting the reading processing in chil- tion, generating whole brain mappings based on the entropy
dren. of each EEG electrode [16, 48, 47] and on non-supervised
The paper is organized as follows. Next, in section 2, and supervised multivariate techniques. The technique of
we provide information about the sample groups selected to EEG summarization is not new and has been successfully
study the reading processing in children based on a public applied to study neural plasticity [16], arithmetic brain pro-
school in Sao Paulo, Brazil. Then, section 3 describes the cessing [48], dermatological treatment satisfaction [2], elec-
technique of EEG summarization and the non-supervised tion decision making [11], DIPS model [9] and, more re-
and supervised multivariate methods used to generate the cently, moral dilemma [10] and medical diagnosis [44].
whole brain mappings for interpreting the reading experi-
ments. All the results of the experiments carried out in this 3.1. EEG signals summarization
work have been explained in section 4. Finally, in section 5,
we conclude the paper, arguing about some ndings high- EEG records the electrical eld potentials generated by
lighted in this work. the activation of sets of neurons or source signals sl lo-
cated in several distinct cortical areas. The EEG data di (t)
recorded at a single electrode i represents a weighted lin-
2. Material ear sum of underlying source signals, that is:
Two sample groups of children were selected from a 
k
public school of the city of Mogi das Cruzes (Sao Paulo, di (t) = wi sl (t). (1)
Brazil), having (DL) and having not (CO) reading difculty i=1
complains by their teachers. The weights wi are determined by the distance of the cor-
A specic anamnesis, which involved the relatives of tical source domains si from the electrode pair, the orienta-
the children, was used to investigate the possible neuro- tion of the cortical patch relative to the electrode pair lo-
logical disturbance of the DL sample group. This anamne- cations, and the electrical properties of intervening tissues.
sis considers environmental factors that could impair brain The number k of active sources is determined by the task
development from the fetal age until early childhood. The being currently processed by the brain.

252
Figure 2. An example of a word reading task carried out in the experiments. Each child has to select
an image (clicking on it) out of the ve shown that best describes the corresponding meaning of the
word presented as written language above the image options.

ci,j calculated for di (t) and dj (t) will approach 1, other-


wise it will approach 0. The highest uncertainty about the
information equivalence provided by ei and ej occurs when
the correlation strength ci,j approaches 0.5.
Therefore, in the same line of reasoning used by Shan-
non [50] to dene the amount of information provided by a
random variable, it is proposed that the informational equiv-
alence h(ci , cj ) of di (t) and dj (t) furnished by ei and ej
is the expected value E(I(ci,j )) of the information I(ci,j )
provided by ci,j [16, 48, 47]. However, because ci,j may
theoretically assume values equal to zero, instead of using
Figure 3. The position of each one of the Shannons logarithm function, the h(ci,j ) estimate has been
20 electrodes according to the 10/20 conven- calculated by:
tional system [32]. The letters F, T, C, P and O
stand for frontal, temporal, central, parietal, h(ci,j ) = E(I(ci,j ))
and occipital lobes, respectively. The mark- = [ci,j log2 (ci,j ) + (1 ci,j )log2 (1 ci,j )].
ers A1 and A2 are used as references to the (2)
midline of the brain.
Now, given q electrodes and the average correlation co-
efcient q1
The statistical complexity of the investigation increases j=1 ci,j
ci = , (3)
as the number of EEG and behavioral variables increase as q1
well. Therefore, it is necessary to summarize the informa- the informational equivalence measured by ci can be writ-
tion provided by each electrode ei about all sources sl into a ten by the following formula
single variable to make statistical analysis amenable. Since
EEG data are assumed to be a weighted sum of the electri- h(ci ) = [ci log2 (ci ) + (1 ci )log2 (1 ci )], (4)
cal activity of the different sources, correlation analysis of
the EEG activity di (t) recorded by the different electrodes which calculates the information provided by di (t) concern-
ei may be used to calculate the entropy information h(ei ) ing that provided by all other dj (t). Thus,
provided by each electrode ei about all k involved sources

q1
si into a single variable [16, 48]. h(ei ) = [h(ci ) h(ci,j )] (5)
The rationality of this process can be briey explained as j=1
follows. Given that data di (t) and dj (t), furnished by two
electrodes ei and ej , provide equivalent information about computes the information provided by di (t) recorded by ei
sources si then the absolute value of correlation coefcient about the sources si . In short, in a cognitive task solving,
we shall expect:

253
over the N trials. Let this data matrix X have sample corre-
lation matrix R with respectively P and eigenvector and
eigenvalue matrices, that is,

P T RP = . (6)
It is a proven result that the set of m (m n) eigen-
vectors of R, which corresponds to the m largest eigenval-
ues, minimizes the mean square reconstruction error over
all choices of m orthonormal basis vectors [18]. Such a set
of eigenvectors scaled by the square root of the correspond-
ing eigenvalues [33] and calculated as
  
L = [ 1 p1 , 2 p2 , ..., m pm ] (7)
is known as the factor loadings of the data matrix X esti-
Figure 4. An illustrative example of an EEG mated by the principal component method.
summarization calculated in the experiments The estimated factor loadings L of X can be rotated in
for the C3 electrode. All the calculations have order to improve the understanding of the factors, specially
been made using the previous 2 seconds im- if R deviates signicantly from a diagonal matrix. If L is
mediately before the decision making. the n m matrix of estimated factor loadings then

F = LT (8)
a) if ci,j = 1 for all ej then ci = 1, h(ci,j ) = h(ci ) for is a nm matrix of rotated estimated factor loadings, where
all ej , and consequently h(ei ) = 0. This indicates that di (t) T is assumed to be an orthonormal m m rotation matrix,
and the corresponding ei do not provide any additional in- that is, T T T = T T T = I.
formation about the sources si ; Ideally, we would like to see a pattern of loadings where
b) if ci,j = 0 for half of ej and ci,j = 1 for the other half, each subset of electrodes is highly represented by a single
then ci = 0.5, h(ci ) = 1, h(ci,j ) = 0 for all ej , and con- factor and has negligible coefcients on the remaining ones,
sequently h(ei ) is maximum and equal to 1. This indicates allowing an interpretation of the EEG brain mappings with
that di (t) and the corresponding ei discriminate two differ- no overlappings. Thus, our natural choice of the orthonor-
ent groups of electrodes providing information about dis- mal matrix T has been based on the varimax criterion pro-
tinct groups of sources si , and posed by Kaiser [34], which has been followed by others in
c) for all other conditions, i.e. 0 < h(ei ) < 1, h(ei ) analogous works [16, 47, 48, 11] .
quanties the information provided by di (t) about the Therefore, those F = [f1 , f2 , ..., fm ] can then replace
sources si . the initial n variables on m rotated common factor load-
Figure 4 shows an illustrative example of an EEG sum- ings where not only the association between the EEG elec-
marization calculated in the experiments for the C3 elec- trodes would be most expressive in terms of variance in-
trode. formation, but also the brain mappings would be the most
independent ones given by the perpendicular rotation T of
3.2. Factor Analysis the initial factor loadings estimated by the principal compo-
nents method.
We have used Factor Analysis (FA), a well-known mul-
tivariate statistical technique, to describe the association 3.3. Linear Discriminant Analysis
between the entropy values of the electrodes in a non-
supervised way. The main idea behind FA is to disclose the The association between the entropy values of the elec-
correlation relationships among the original variables using trodes in a supervised way has been performed here using
a few unobservable random ones, called common factors, to Linear Discriminant Analysis (LDA) and the technique of
adequately represent the data [33]. hyperplane navigation [54, 20, 49]. The primary purpose of
In particular, let an N n data matrix X be composed of LDA is to separate samples of distinct groups by maximiz-
N input signals (or trials) with n variables (or electrodes). ing their between-class separability while minimizing their
This means that each column of matrix X represents the within-class variability.
EEG summarization of a particular electrode observed all Let the between-class scatter matrix Sb be dened as

254

g
Sb = Ni (xi x)(xi x)T (9)
i=1
and the within-class scatter matrix Sw be dened as


g 
g 
Ni
Sw = (Ni 1)Si = (xi,j xi )(xi,j xi )T ,
i=1 i=1 j=1
(10)
where xi,j is the n-dimensional signal (or trial) j from class
i , Ni is the number of trials from class i , and g is the to-
tal number of classes or groups. The vector xi and matrix Si
are respectively the unbiased sample mean and sample co-
variance matrix of class i [18]. The grand mean vector x
Figure 5. Brain mapping of the most expres-
is given by
sive factor loadings of the CO sample group
with corresponding eigenvalues greater than
1  1 
g g Ni
x= Ni xi = xi,j , (11) 1.
N i=1 N i=1 j=1
where N is, as described earlier, the total number of input
signals, that is, N = N1 + N2 + . . . + Ng . As can be seen from Figure 5, FA using the entropy in-
The main objective of LDA is to nd a projection ma- formation from the CO sample group has disclosed three
trix Wlda that maximizes the ratio of the determinant of patterns of cortical neural organization. The common fac-
the between-class scatter matrix to the determinant of the tor 1 (f1, on the left) discloses a higher loading value to
within-class scatter matrix (Fishers criterion), that is, electrodes FP1, FP2, FZ, F7 and F8; the common factor 2
 T  (f2, in the middle) has clustered T4, T5, T6 and PZ; and
W S b W 
Wlda = arg max T . (12) the common factor 3 (f3, on the right) shows the connection
W |W Sw W | between CZ and C3. In words, f1 shows a bilateral high
The Fishers criterion described in equation (12) is max- correlated activity at the anterior brain that may be asso-
imized when the projection matrix Wlda is composed of the ciated with the reading executive functions [3, 14], target
1
eigenvectors of Sw Sb with at most (g 1) nonzero cor- word loading in the working memory and the temporal and
responding eigenvalues [18, 13]. In the case here of a two- spatial eye scanning control of the possible matching words
class problem, the LDA projection matrix is in fact the lead- or gures. The second factor, f2, shows a bilateral corre-
1 lated activity at the temporal brain that may be associated
ing eigenvector wlda of Sw Sb .
Once the leading eigenvector wlda has been computed, with both the visual recognition of words and gures and
we can move along its corresponding projection vector the associated meaning processing [56, 40, 57]. The last fac-
and extract simultaneously the discriminant differences cap- tor considered, f3, discloses a relation between medial and
tured by the entropy of each EEG electrode. In mathemat- left central electrodes possibly associated to decision mak-
ical terms, assuming that the spreads of the sample groups ing. It is important to note that the bilateral association dis-
follow a Gaussian distribution, this procedure of navigating closed by the rst two common factors (f1 and f2) is in ac-
on the most discriminant projection [54, 20, 49] can be gen- cordance with the fact that our word/phrase reading tasks
erated through the following simple expression: involved both visual (a preferential right hemisphere func-
tion) [29, 30, 25] and verbal (the left hemisphere special-
yi,j = x + ji wlda , (13) ization) [26, 27, 28] processing and association of these re-
where j {3, 2, 1, 0, 1, 2, 3} and i is the standard sults.
deviation of each sample group i {1, 2}. However, from Figure 6, it is possible to see that using
the entropy information from the DL sample group FA has
4. Results disclosed only two patterns of brain activity for word/phrase
reading solution in children with learning difculties. The
Figures 5 and 6 describe the rotated estimated factor common factor 1 (f1, on the left) of Figure 6 discloses a
loadings of the neural organization of the CO and DL sam- high correlated bilateral anterior activity encompassing a
ple groups, respectively, with corresponding eigenvalues greater amount of sources than factor 1 of CO group. Here
greater than 1. it consumes resources from basically all central and frontal
brain but the prefrontal. This could be in accordance with

255
with the verbal sounds they achieved to translate through the
grapheme-phoneme conversion.

5. Discussion

In this work, we have used EEG and multivariate statis-


tical analysis to disclose cortical neural organization of dif-
ferent groups of children having distinct performances on
word/phrase reading tasks.
Given the design of the reading task we should expect
the recruitment of at least the following three main cogni-
tive functions: verbal to read (words), visual to recognize
Figure 6. Brain mapping of the most expres- (images) and executive to control attention between the var-
sive factor loadings of the DL sample group ious information stimuli carried out (1 target word and 5
with corresponding eigenvalues greater than image options). Since the work from Baddeley [3], it has
1. been suggested that our working memory, that is, our abil-
ity to deal with various information for a short period of
time, involves three components which comprise the tem-
the fact that these individuals, being unable to disclose the poral verbal-acoustic storage system, the visual sketchpad
meaning of the words, had to compute much more executive and the central executive, having each one of these compo-
functions in controlling the possible associations between nents a respectively major correspondence to left, right and
the images processed by right neurons and the sounds they frontal-prefrontal brain areas.
could produce from their poor grapheme-phoneme conver-
Therefore, based on our DL sample group results and
sion operated at left neurons. In factor 2 (f2, on the right)
linking the briey mentioned Baddeley model with the
we see a strong covariation at the posterior and prefrontal
dual-route reading language model, we may argue that:
brain, enrolling the temporal T5 and T6 and occiptal O1
(factor 1) the temporal verbal-acoustic storage system and
and O2 regions. This association may be related with the at-
the visual sketchpad were associated trying to correlate
tempt to associate meaning to the target written word di-
the sounds produced by the left frontal neurons during
rectly from the visual analysis of the possible matching
grapheme-phoneme conversion to the image options and
gures by the lexical route but demanding executive ef-
positions processed by the right central frontal areas; (fac-
forts from prefrontal neurons showing a not well established
tor 2) the occipital-temporal lexical route needed the en-
temporo-occiptal integration. From these two maps we may
rollment of pre-frontal neurons in order to use the central
argue that this group tried to use both reading routes, but
executive to coordinate the interaction between the word-
disrupted one from another, failing in use executive func-
reading area (temporal neurons) and the visual occipital
tions to coordinate the interaction between them.
neurons.
Lastly, the LDA brain mapping is shown in Figure 7.
LDA hyperplane navigation has disclosed a left to right dif- As a nal consideration, the differences found between
ferentiation between CO and DL, grouping mainly the left both sample groups, i.e. the number of factors with eigen-
central and prefrontal regions of the electrodes C3 and FP1 values greater than 1 and the left to right regions discrimi-
on CO group and the right central and frontal regions of the nating CO and DL children, show that the set of techniques
electrodes C4 and F8 on the DL group. In other words, LDA used here to generate the brain mappings may become an
showed that what most discriminated controls from those effective tool in helping the diagnostic process of children
with reading difculties might have been the activity on lan- with learning disabilities. We believe that these mappings
guage/reading circuits located on left hemisphere, whereas used jointly with an anamnesis and a set of cognitive tasks
right activity, possibly associated to visual processing of the may at least help us better understand the neural organiza-
image options, discriminated the children with reading dif- tion underlying the ability to solve different kinds of prob-
culties. According to the fact that DL children did not re- lems by different sample groups.
trieve the meaning of the words, it might be suggested that Finally, we want to remark that we aim to expand this
this group relied less on language circuits to solve the task study investigating a larger group of children enrolled at two
and more on visual processing trying to nd out what im- public schools located at a region of northeast of Brazil on
age could be selected by examining and comparing each one risky of social exclusion.

256
Figure 7. Brain mapping of the most discriminant entropy values captured by the LDA
hyperplane navigation. From left (group of CO samples) to right (group of DL samples):
[31 , 21 , 11 , x1 , +11 , boundary, 12 , x2 , +12 , +22 , +32 ].

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(306392/2011-9). Burattini. Neurodynamics of an election. Brain Research,
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