Appl Psychophysiol Biofeedback
DOI 10.1007/s10484-015-9309-6
Neurofeedback in Learning Disabled Children: Visual
versus Auditory Reinforcement
Thalı́a Fernández1 • Jorge Bosch-Bayard1 • Thalı́a Harmony1 • Marı́a I. Caballero2
Lourdes Dı́az-Comas3 • Lı́dice Galán3 • Josefina Ricardo-Garcell1 •
Eduardo Aubert3 • Gloria Otero-Ojeda4
Ó Springer Science+Business Media New York 2015
Abstract Children with learning disabilities (LD) fre-
quently have an EEG characterized by an excess of theta
and a deficit of alpha activities. NFB using an auditory
stimulus as reinforcer has proven to be a useful tool to treat
LD children by positively reinforcing decreases of the
theta/alpha ratio. The aim of the present study was to
optimize the NFB procedure by comparing the efficacy of
visual (with eyes open) versus auditory (with eyes closed)
reinforcers. Twenty LD children with an abnormally high
theta/alpha ratio were randomly assigned to the Auditory or
the Visual group, where a 500 Hz tone or a visual stimulus
(a white square), respectively, was used as a positive
reinforcer when the value of the theta/alpha ratio was
reduced. Both groups had signs consistent with EEG mat-
uration, but only the Auditory Group showed behavioral/
cognitive improvements. In conclusion, the auditory rein-
forcer was more efficacious in reducing the theta/alpha
ratio, and it improved the cognitive abilities more than the
visual reinforcer.
& Thalı́a Fernández
thaliafh@yahoo.com.mx
1
Departamento de Neurobiologı́a Conductual y Cognitiva,
Instituto de Neurobiologı́a, Universidad Nacional Autónoma
de México, Campus Juriquilla, Boulevard Juriquilla 3001,
76230 Juriquilla, Querétaro, Mexico
2
Facultad de Psicologı́a, Universidad Autónoma de Querétaro,
Querétaro 76010, Mexico
3
Centro de Neurociencias de Cuba, Avenida 25 y 158, Playa,
La Habana, Cuba
4
Facultad de Medicina, Universidad Autónoma del Estado de
México, 50180 Toluca, Mexico
•
Keywords Neurofeedback  Visual versus auditory
reinforcement  Learning disabled children  QEEG 
EEG-biofeedback
Introduction
Learning disabilities (LD) are one of the most frequent
problems that afflict children in elementary school
(American Psychiatric Association 2000). LD are diag-
nosed when an individual’s achievement on individually
administered, standardized tests in reading, mathematics,
or written expression is substantially below that expected
for age, schooling, and level of intelligence. LD are clas-
sified as ‘‘specific’’ (reading disorder, mathematics disor-
der, or disorder of written expression) or ‘‘learning disorder
not otherwise specified,’’ which might include problems in
all three areas (American Psychiatric Association 2000).
Children included in this study belonged to the latter group.
Although LD children often have some deficit in atten-
tional processes, children in our study did not satisfy the
criteria to be classified as Attention Deficit Hyperactivity
Disorder (ADHD), and no one was hyperactive.
The EEG of LD children is characterized by slower
activity, principally in the theta range, and less alpha
activity than normal children of the same age (Chabot et al.
2001; Fernández et al. 2002; Fonseca et al. 2006; Gasser
et al. 2003; Harmony et al. 1990; John et al. 1983);
therefore, an adequate NFB protocol could be to reward
reduction of the theta/alpha ratio in the region with the
highest ratio.
According to the review of Cantor and Chabot (2009),
so far only three published articles have explored the
effects of NFB in this population: Fernández et al. (2003),
Becerra et al. (2006) and Fernández et al. (2007). These
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three studies have in common the following features:
(a) children with LD had delayed maturation of their EEG,
expressed as an abnormally high theta/alpha ratio, (b) the
protocol used positively reinforced reduction of the theta/
alpha ratio, and (c) the reinforcement was an auditory
stimulus (tone of 500 Hz and 60 dB). More recently, other
studies have been conducted in similar populations, such as
children with dyslexia (Breteler et al. 2010) and children
with LD (Nazari et al. 2012), using different NFB protocols
that involve mainly EEG coherences. In the first one, the
sensorial modality of the reinforcers was not reported; in
the second, video games were used as feedback, but it was
not reported if accompanying sound was also included.
These facts show the lack of importance given to this
aspect of treatment.
In clinical practice a visual stimulus is often used as
reinforcement when a NFB treatment is given. It is logical
to proceed in such a way, because in humans there is visual
dominance, i.e., in bimodal environments vision often has
an advantage over other senses, and visual dominance
emerges because the visual system is less vulnerable to
competition than the auditory domain (Schmid et al. 2011).
However, in NFB learning, different sensory modalities as
reinforcers have not been compared to determine which
stimulus would provide optimal training.
In tasks of Reaction Time (RT) most of the results
support the superiority of the auditory over the visual
modality. Thompson et al. (1992), Shenvi and Balasubra-
manian (1994), Pain and Hibbs (2007), Shelton and Kumar
(2010), and Ng and Chan (2012) have documented that the
auditory RT is faster than the visual RT; in contrast, Ver-
leger (1997) and Yagi et al. (1999) showed that the visual
RT is faster than the auditory. McAuley and Henry (2010)
examined modality effects in rhythm processing using a
tempo judgment paradigm, finding that auditory rhythms
demonstrate an advantage over visual rhythms; analo-
gously, Bueno and Ribeiro do Valle (2012) studied the
effect produced by the warning stimulus modality in a
reaction time task, and they found that an auditory warning
stimulus exerts a stronger inhibitory influence on respon-
sivity than a visual warning stimulus. In contrast, visual
temporal reference memory may be more permanent than
auditory reference memory, although auditory temporal
information and visual temporal information do not
mutually interfere in reference memory (Ogden et al.
2008). Since NFB is a learning procedure, the aim of this
study is to evaluate whether, in the treatment of NFB that
reinforces the reduction of the theta/alpha ratio, there is
some effect of the modality of reinforcement on the EEG
and cognitive results, and if so, to determine which
modality, auditory or visual, is better to treat children with
LD and an abnormally high theta/alpha ratio. Note that the
treatment using the auditory reinforcer was administered
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Appl Psychophysiol Biofeedback
with eyes closed as opposite to the treatment with the
visual reinforcer, administered with eyes open; which
mixes two effects in our experiment.
Because (a) EEG alpha activity is higher in the absence
of sensory stimulation, for example, when the eyes are
closed (Riviello et al. 2011), (b) auditory stimulation pro-
duces faster cortical activation than visual stimulation
(Pain and Hibbs 2007), and (c) children with Reading
Disability show abnormal activity during semantic pro-
cessing in the visual but not in the auditory modality
(Booth et al. 2007; Liu et al. 2010), we hypothesized that to
apply NFB using an auditory stimulus (and with eyes
closed) as reinforcement could be more effective than to
use a visual stimulus (with eyes open).
Methods
The Ethics Committee of Instituto de Neurobiologı́a,
Universidad Nacional Autónoma de México approved the
experimental protocol.
Participants
One hundred and eighty-seven children between 6 and
12 years of age were referred by a social worker from
several elementary schools in Querétaro. Twenty children
fulfilled the following inclusion criteria: LD children with
normal neurological exam, Intelligence Quotient (IQ)
greater than 70 (IQ was assessed by the revised version of
the Weschler Intelligence Scale for Children, WISC-R,
Weschler 1981), mother with at least a third-grade ele-
mentary school education, per capita income greater than
50 % of the minimum wage, and an EEG recorded at rest
with eyes closed in which at least one lead showed an
abnormally high value of the theta/alpha ratio compared to
a normative database (Valdés et al. 1990, see below).
Children with paroxysmal activity in the alpha frequency
range were excluded in order to avoid the risk of increasing
this abnormal activity when reduction of theta/alpha ratio
was positively reinforced. Children with an ADHD diag-
nosis or another psychiatric alteration were also excluded.
A team composed of a neurologist, a neuropediatrician,
and a clinical psychologist evaluated the children to
establish the ‘‘LD not otherwise specified’’ diagnosis
according to the DSM IV criteria (American Psychiatric
Association 2000). The tests used were the arithmetic
subscale of the WISC-R and a writing-reading test stan-
dardized by grade for Mexican children (Iglesias and
Derman 1985). In addition, clinical characteristics of the
child and his/her academic achievement were taken into
account. Subjects included in this study were classified as
children with ‘‘learning disorder not otherwise specified’’;
Appl Psychophysiol Biofeedback
several of them presented problems in attentional pro-
cesses, as is common in this population (Bernal et al. 2000;
Holcomb et al. 1986; Silva-Pereyra et al. 2003), but they
did not meet the DSM-IV criteria for ADHD (American
Psychiatric Association 2000). In addition, cranial com-
puted tomography was performed on each child in order to
exclude those with major brain abnormalities. Children
excluded from the sample were sent to a specialized service
or included in another research project.
Children were randomly assigned to one of two groups
of ten. Children from one group received the NFB treat-
ment using as reinforcement an auditory stimulus (Audi-
tory Group, AG), and children of the other group received a
NFB treatment using as reinforcement a visual stimulus
(Visual Group, VG). Before treatment, no significant dif-
ferences between groups were observed in age (AG:
9.10 ± 1.24, VG: 9.08 ± 1.61, mean ± SD), gender (AG:
6 F and 4 M, VG: 5 F and 5 M), or ADHD score from
TOVA (AG: -2.73 ± 2.73, VG: -1.14 ± 2.13, mean ±
SD). Significant differences were observed in IQ (AG:
76.91 ± 9.47, VG: 94 ± 16.23, mean ± SD, p = 0.01).
All children were volunteers; parents’ and children’s
informed consent were obtained in all cases.
No control group was included in the present study,
because in previous studies (Becerra et al. 2006; Fernández
et al. 2003) the protocol using an auditory stimulus had
been compared with a sham control group, demonstrating
that the auditory NFB protocol is useful to treat LD chil-
dren with a lag in EEG maturation.
Procedure
Before treatment, two or three EEG recordings were taken
from each child in order to select the lead where the most
abnormal Z value of the theta/alpha ratio was found. NFB
was applied based on the EEG activity at this lead. The last
EEG recording before treatment was used as ‘‘before’’ in
the statistical analysis, because the first EEG recording
could have been affected by the environment being novel
for the child.
WISC-R and the parent interview (see below) were
carried out before treatment and used as inclusion criteria.
The Test of Variables of Attention (TOVA; Leark et al.
1999) in its visual mode was also applied, but it was not
used as an inclusion criterion.
About 2 months after the 20 treatment sessions (with
auditory or visual reinforcement), the TOVA and EEG
were repeated following the same procedures as before
treatment. A second WISC-R was administered at least
6 months after the first one, in accord with WISC-R rec-
ommendations. A final interview with the parents was also
conducted in order to obtain their qualitative evaluation of
behavioral changes. Academic achievement was commu-
nicated by the parents.
Behavioral Assessment
WISC-R
WISC-R is one of the most-used instruments in assessing
children’s intelligence and general cognitive functions. It is
a collection of 13 distinct subtests divided into two scales
(a Verbal scale and a Performance scale). Five of the
subtests in each scale produce scale-specific IQs, and the
10 subtest scores produce a Full Scale IQ (Weschler 1981).
In this study WISC-R was used to exclude mental
retardation and to assess the arithmetic performance (only
in this sense did it contribute to the LD diagnosis). It also
was used to determine, together with the data derived from
TOVA and parent interviews, if children treated with NFB
showed a cognitive improvement.
TOVA
TOVA in its visual mode was administered to all children.
TOVA is a computerized, continuous performance test in
which the subject has to respond to a target that is pre-
sented less frequently than non-target stimuli in the first
half of the test, and more frequently in the second half. The
‘‘ADHD score’’ is the index of the TOVA that tells how
similar the performance is to that of the ADHD profile
(Leark et al. 1999).
Interview of Parents
An experienced clinical psychologist interviewed the
mother, father, or tutor of the child guided by an ad hoc
questionnaire to evaluate socioeconomic status (mother
schooling and per capita income are inclusion criteria) and
family integration, psychomotor and emotional develop-
ment, social interaction, cognitive abilities, academic
achievement, and pathologic history of the child. This
interview had two objectives: (a) as an inclusion criterion,
and (b) to record the parents’ qualitative observations of
changes after treatment regarding attention, memory,
learning, behavior, attitude toward school, social interac-
tion, and emotional changes of the child.
EEG
The EEG was recorded with two purposes: (a) as an
inclusion criterion (the subject should have at least one lead
with an abnormally high value of the theta/alpha ratio, and
he/she should not present paroxysmal activity in the alpha
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range), (b) to compute the Absolute and Relative Power in
the delta (1.56–3.52 Hz), theta (3.91–7.42 Hz), alpha
(7.81–12.50 Hz), and beta (12.89–19.14 Hz) frequency
bands in two conditions: before and after NFB treatment.
MEDICID IV, the equipment used to record the EEG, was
also used to analyze the EEG records and to give the NFB.
This equipment was developed by Neuronic A.C., and has
been used in numerous studies. The norms (Valdés et al.
1990) and the description of the NFB program (Fernández
et al. 2003) will be described below.
EEG Recording and Editing
Subjects were seated in a comfortable chair in a dimly lit
room. Digital EEG was recorded at rest with eyes closed for
20 min from 19 leads (10–20 International System) using
linked ear lobes as reference. A1A2 reference was used in
order to maintain the same conditions as in the normative
data. The amplifier bandwidth was set between 0.5 and 30 Hz.
The EEG was sampled every 5 ms using the MEDICID IV
System and edited off-line. An expert electroencephalogra-
pher using visual editing selected twenty-four artifact-free
segments of 2.56 s for quantitative analysis.
EEG Analyses
The EEG analyses were done off-line. The fast Fourier
transform and cross-spectral matrices were calculated every
0.39 Hz, and the absolute power (AP) in the theta
(3.6–7.5 Hz) and alpha (7.6–12.5 Hz) bands was computed.
The ranges of these bands were selected according to nor-
mative data provided by MEDICID IV. Population param-
eters of the normative data were based on the regression
function of age-dependent mean values and the standard
deviation obtained from 211 normal subjects between 6 and
90 years old; the ages were distributed in logarithmic form;
thus, subjects are concentrated in the age range considered in
the present paper (Valdés et al. 1990, 1992).
Z Values for the theta/alpha Ratio
Z values for the theta/alpha ratio were calculated in the
following manner: AP in each band was computed for the
average reference, and the geometric power (Hernández
et al. 1994) was subtracted from the cross-spectral matrix.
The value ‘‘log (theta AP/alpha AP)’’ was computed, and Z
values for this logarithm were calculated using the
equation:
Z ¼ ½logðthetaAP=alphaAPÞ  l=r
where l and r are the mean value and the standard devi-
ation of the normative sample of the same age as the
subject, respectively. Taking into account that the EEG
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Appl Psychophysiol Biofeedback
abnormality considered in this population is a high value of
the theta/alpha ratio, it was deemed that Z should be greater
than 1.645 to be considered as abnormal (this Z value
corresponds to a 1-tail distribution, p = 0.05). The pres-
ence of at least one abnormal value in one lead was an
inclusion criterion. Treatment was given via the lead with
the highest abnormal value.
NFB Treatment
NFB was conducted using an NFB program adapted to the
MEDICID IV recording system and software. The EEG
recording was obtained from the lead with the most
abnormal theta AP, referred to the linked earlobes. A
threshold level was selected every three min such that the
subject obtained a reward between 60 and 80 % of the
time. Depending on the group, the child received a visual
or an auditory stimulus as reward. The auditory stimulus
was a tone of 500 Hz at 60 dB, and the visual stimulus was
a white square of 20 cm2 over a black background of a
computer monitor. The AG children received treatment
with their eyes closed, while the VG children received it
with their eyes open.
Throughout the recording, the ratio was computed for
1280 ms every 20 ms, i.e. using overlapped windows, and
compared with the threshold. If the ratio was lower than the
threshold, the reward was given. Subjects were told that it
was important to maintain the duration of the tone as much
as possible, and consequently the tone acquires a positive
meaning.
Each child received 20 sessions of training, around two
per week (each of which lasted 30 min), over a period of
10–12 weeks. At the beginning of each session, the child
was told that if his/her performance was good, he/she
would receive candy at the end of the session.
Statistical Analysis
Sample sizes were small, and a normal distribution was not
guaranteed; thus, parametric analyses were inappropriate.
To control for Type I error, a non-parametric permutational
ANOVA model was used (Pesarin and Salmaso 2010). A
two-way ANOVA was estimated using as factors group
(AG vs. VG) and time (before vs. after NFB treatment).
The global test is calculated under the permutation distri-
bution of the maximum of the F statistic. The interaction
was considered to determine if the change produced by
NFB was equal or different between groups. Multiple
comparisons were carried out by computing all pairwise
comparisons using the Student’s t test (Galán et al. 1997).
These mass-univariate methods have been employed to
determined changes between before and after treatment in
each group.
Appl Psychophysiol Biofeedback
Usually, the contrasts of ANOVA are only analyzed in
the variables where the interaction effect is significant;
however, in this study all changes between before and after
treatment in each group were of interest, including those in
which the interaction effect was not significant; therefore,
the marginal hypotheses were evaluated as a contrast of
ANOVA for each lead. Analyses of the behavioral data
were performed in an analogous manner, and scores from
the WISC-R and TOVA were considered separately. The
theta/alpha ratio in the most abnormal lead was also
analyzed.
Results
As the children were randomly assigned to the two groups,
it is important to determine whether there were pretreat-
ment differences between groups; therefore, each ANOVA
will be preceded by a comparison between groups before
NFB treatments.
Z Value of theta/alpha Quotient in the Lead Selected
to Give NFB Treatment
The Z value of the theta/alpha quotient in the lead selected
to give NFB treatment did not present significant differ-
ences between groups before treatment (AG:2.16 ± 0.35;
VG:2.44 ± 0.47). In the AG, 6 of these leads were located
in the left hemisphere and 4 in the right hemisphere; in the
VG, 7 leads were located in the left hemisphere, 2 in the
right hemisphere, and 1 at the midline.
The ANOVA of Z values of the theta/alpha quotient in
the most abnormal lead showed no significant differences
in the main effect for Group or for the Time 9 Group
interaction, but a significant main effect for Time was
found (p = .002). This means that, regardless of which
group, significant differences were observed between
before and after treatment. Post hoc analyses revealed a
significantly reduced Z value of the theta/alpha quotient
both in the Auditory (p \ .01) and Visual (p \ .01) group,
confirming the ANOVA significance result.
During the NFB session, the reward percentage was
rarely observed to be lower than 60 % in all subjects. In 9
subjects of each group, the Z value of the theta/alpha ratio
decreased after treatment in the lead in which NFB was
given (in one subject it remained unchanged); this ratio
reached normal values after treatment in 7 of the 10
children in the AG, but in only 3 of the VG subjects. The
effect size in the AG was significantly higher than that in
the VG (Odds ratio = 5.44, 95 % confidence interval
0.80–36.86, both calculated following Cummings (2014)
software).
Behavioral and Cognitive Results
Before treatment, significant differences between groups
were observed. Children of the AG had a significantly
greater Average Response Time in the TOVA (p = 0.04),
and a significantly lower Performance IQ (p \ 0.01) and
Total IQ (p = 0.01) than children of the VG.
To compare the effect of the treatment between groups,
we performed ANOVAs. The ANOVAs that included
WISC-R variables showed no significant differences in the
main effect for Time or for the Time 9 Group interaction,
but a significant main effect for Group was found for Total
IQ (p \ .001) and Performance IQ (p \ .001). The AG had
higher scores for both IQ measures.
The ANOVAs that included TOVA variables showed no
significant differences in main effect for Time. A main
effect for Group was found in Commission Errors
(p = .025) and Average Response Time (p = .027), and a
significant Time 9 Group interaction was found for the
ADHD score (p = .012) and Omissions (p = .029). The
post hoc analyses, considering the groups separately, are
shown in Figs. 1 and 2 for WISC-R and TOVA results,
respectively. In the AG, Verbal IQ and Total IQ from
WISC-R increased after treatment (p \ 0.01 and p = 0.01,
respectively), while in TOVA, AG exhibited a decrease of
the Commission Errors (p \ 0.01) and an increase of the
ADHD score (p \ 0.01); a tendency to reduction of the
Average Response Time was also observed (p = 0.06). In
the VG no significant changes were observed, although
there was a general tendency to improve behavior and
cognition. The strongest tendency was observed in the
reduction of the Average Response Time (p = 0.06).
Parents of children of the both groups reported similar
positive changes in attention, memory, and self-esteem;
they saw that their children had more enthusiasm for
school, and that they received better scores. Parents also
observed less shyness and passivity in their children, which
improved their relationships with their classmates.
EEG Results
Before treatment, many differences between groups were
observed. Global delta (p = .02) and alpha (p = .05)
absolute power (AP) values were higher in the AG than in
the VG. Marginal results indicated that differences occur-
red in Fp1, Fp2, C3, C4, and Cz for delta AP; Cz for theta
AP; C3, P3, T5, and Cz for alpha AP; and Fp1, F3, F8, Fz,
and Cz for beta AP. Global comparisons for relative power
(RP) were not significant, but the AG had higher values
than the VG in O2 and T6 for delta RP, and in P3 and Pz
for alpha RP; the AG had lower values than the VG for beta
RP in Cz (Table 1).
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 Appl Psychophysiol Biofeedback

Fig. 1 Means and standard errors of Verbal IQ, Performance IQ, and in the Visual Group, but the Verbal IQ (p \ 0.01) and Total IQ
Total IQ from the WISC-R in the Auditory and the Visual Groups. No (p \ 0.05) increased significantly in the Auditory Group
significant differences between before and after NFB were observed

Fig. 2 Means and standard errors of Omissions, Commissions, before and after NFB were observed in the Visual Group, but in the
Average Response Times, and ADHD scores from the TOVA in the Auditory Group significant decreases of Commissions (p \ 0.01) and
Auditory and the Visual Groups. No significant differences between ADHD scores (p \ 0.01) were observed

Table 1 EEG significant

AG \ VG AG [ VG
differences between groups
before NFB treatments Global p Significant leads p \ .05 Global p Significant leads p \ .05

Absolute power
delta .02 Fp1, Fp2, C3, C4, Cz
alpha .05 C3, P3, T5, Cz
beta Fp1, F3, F8, Fz, Cz
Relative power
delta O2, T6
alpha P3, Pz
beta Cz

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Appl Psychophysiol Biofeedback
The ANOVAs that showed significant differences for
the Time 9 Group interaction were delta AP (p = .027),
alpha AP (p \ .0009), and beta RP (p = .021). The prin-
cipal leads involved in these differences were Cz for delta
AP and beta RP; and O1, Fz, and Cz for alpha AP.
Changes considering groups separately are shown in
Figs. 3, 4 and 5. In both groups, delta and theta AP and RP
decreases and alpha AP and RP increases were observed, as
well as an increase in beta AP and RP, mainly in the AG.
However, qualitative differences, mostly topographic, in
the pattern of change were observed between groups. Delta
reduction was seen in frontal leads of both groups, but in
addition, the AG showed a delta AP and RP decline in
posterior leads; a theta AP reduction was found in fron-
totemporal leads in both groups; however, in the AG, theta
AP also decreased in posterior regions. Although theta and
alpha RP changes were similar for AG and VG, the topo-
graphic distribution of the alpha AP increase was different:
in the AG changes were observed in frontal areas, and in
the VG changes were found in frontal and parietooccipital
regions. With respect to the beta band, an increase of beta
RP was observed only in the AG, and more centroparietal
leads were involved in the beta AP increase in the AG.
Discussion
In this study, and for any NRA protocol in general, great
importance must be given to the stimulus used as a rein-
forcer; therefore, very simple stimuli for both modalities
were chosen. In operant conditioning, a more efficient
learning is associated with a higher contingency between
the reinforcer and the response; a simpler stimulus, such as
a tone or a flash, allows this contingency to be greater
Fig. 3 Significant differences (p \ 0.05) in Absolute and Relative Power between before and after NFB treatment. Blue and red arrows
represent a decrease and an increase of the value, respectively, in the lead in which they are positioned
(Stevenson and Wright 1966). More complex stimuli
would require a longer time for analysis, reducing their
efficiency to induce conditioning, which is accentuated in
the population under study, because as has been reported,
children with learning disabilities have a lower processing
speed (Catts et al. 2002; Neville et al. 1993).
The hypothesis of this study was that learning-disabled
children who received NFB using an auditory reinforcer
would have better learning than children trained with a
visual reinforcer. The main indicator of the NFB learning is
the parameter that is modified by the NFB, in this case the
Z value of theta/alpha quotient in the lead in which it
reached the most abnormal value. In both groups this
quotient was significantly reduced by the training; how-
ever, more children with normalized Z theta/alpha values
were found in the AG after treatment, in spite of the fact
that before treatment they had more EEG abnormalities.
For these reasons it is possible to affirm that suppression of
theta/alpha ratio had a more dramatic effect in the AG.
Additionally, although children of the AG had worse scores
before treatment, behavioral changes that represent a cog-
nitive improvement were significant only in the group that
received NFB with auditory reinforcement (their ADHD
score and commissions decreased, and their verbal and
total IQs increased). These two facts suggest that the NFB
given using the auditory reinforcer was more effective.
Although the auditory and visual reinforcers produced
different behavioral and cognitive results, they produced
similar EEG changes. The auditory reinforcer produced a
greater reduction of posterior delta and theta activity,
suggesting a greater acceleration of the EEG maturation. In
both groups, an increase in frontal alpha activity was
observed. Increased frontal alpha activity has been
described in two populations: ADHD children (Chabot
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 Appl Psychophysiol Biofeedback

Fig. 4 Average power spectra of the Auditory (a) and Visual (b) Groups, in two conditions: before (red line) and after (blue line) NFB treatment

et al. 2005; Chabot and Serfontein 1996; Ricardo-Garcell
2004) and older adults (Riviello et al. 2011). In the former,
it is presumed to be a sign of compensation and could be
the same in the older population as well. The increase in
frontal alpha activity observed here in NFB-treated LD
children using an auditory stimulus may also represent a
compensatory phenomenon, i.e., a reorganization of brain
function to perform tasks; if this is true, then the increased
frontal alpha activity could also explain the cognitive
improvement of these children. In the VG the increase of

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Fig. 5 Average Absolute Power maps of the Auditory (upper) and
Visual (bottom) groups, before (red) and after (blue) NFB treatment.
Observe the theta reduction and alpha increase in both groups after
alpha activity was also observed in the posterior regions
where the visual stimuli are processed; this increase may
also indicate a reorganization of the visual cortices, and it
may also be considered a maturational improvement since
it increases with age during development (Dı́az de León
et al. 1988; John et al. 1980; Matousek and Petersén 1971).
Furthermore, the increase in beta activity was clearly
observed only in the AG, and this occurred in central
regions. The increase in low frequencies of the beta band in
these regions could be an increase of the sensorimotor
rhythm, which could have been revealed although it had
not been reinforced, as often happens in the brain reorga-
nization produced by this type of treatment. The sensori-
motor rhythm increase (Thompson et al. 2010) or the slow
beta increase (Lubar et al. 1995) could also explain the
improvement in the attention spectrum, reflected in the
TOVA, and even in the IQ.
An auditory stimulus usually takes 8–10 ms to reach the
brain, whereas a visual stimulus takes between 20 and
the treatment; in addition, the maps show delta decreases in the
Auditory Group, and beta increases in the Visual Group, after the
treatment
40 ms (Pain and Hibbs 2007). As the information provided
by an auditory stimulus reaches the cortex faster than that
from a visual stimulus, when an auditory reinforcer is given
the contingency is higher than when a visual stimulus is
given. This may explain why the learning acquired by
auditory reinforcement is better than that acquired by
visual reinforcement.
It may be necessary for future studies to use a pseudo-
random method instead of a random method to assign
subjects to different groups when the sample size is small,
in order to reduce initial differences between groups. Since
in our study we randomly assigned subjects to the groups,
significant differences were observed between groups
before treatment in cognitive and EEG variables. This is a
confounding factor which makes it more difficult to inter-
pret the results.
In the present experiment the sensory modality of the
reinforcer was not the unique difference between the two
NFB protocols; effects that may have been caused by the
123

modality are confounded by the fact that in the AG the eyes
were closed while in the VG they were open. One might
think that there is a higher EEG signal-to-noise ratio during
eyes closed than during the eyes open condition; however,
an advantage of using this ratio is that it does not include
the principal sources of noise that commonly interfere in
EEG recordings: electromiogram and electrooculogram,
observed in beta and delta frequency bands, respectively.
More than an increase in the signal-to-noise ratio, it seems
that the fact that the subject remains with closed eyes might
favor the production of alpha. This has to be explored in
future studies, because it constitutes a limitation of the
present work.
Conclusion
Treating children with learning disabilities and abnormal
theta/alpha values by giving NFB using a protocol that
reinforces the reduction of the theta/alpha ratio is more
effective when auditory rather than visual stimuli are
used.
Acknowledgments The authors are grateful for the children’s and
parents’ cooperation in this study. The authors also acknowledge
Judith Becerra, Fabiola Garcı́a, Nelson Pumariega, Héctor Belmont,
Susana Angélica Castro-Chavira, Lourdes Lara, Leonor Casanova,
Bertha Esquivel, Teresa Álvarez, Marı́a Elena Juárez, Eneida Porras-
Kattz, and Efraı́n Santiago for technical assistance, Roberto A. Prado-
Alcalá for his invaluable psychological comments, and Dorothy Pless
for revising English style. This project was supported in part by
Grants IN226001, IN204103 and IN204613 from PAPIIT; 2001 and
E59 from CONCYTEQ; and 69145 and 218556 from CONACYT.
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