Neurofeedback in Learning Disabled Children: Visual

Neurofeedback in Learning Disabled Children: Visual versus Auditory Reinforcement Thalía Fernández, Jorge Bosch-Bayard, Thalía Harmony, María I. Caballero, Lourdes Díaz-Comas, Lídice Galán, Josefina Ricardo-Garcell, et al. Applied Psychophysiology and Biofeedback In association with the Association for Applied Psychophysiology and Biofeedback ISSN 1090-0586 Appl Psychophysiol Biofeedback DOI 10.1007/s10484-015-9309-6

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Author's personal copy Appl Psychophysiol Biofeedback DOI 10.1007/s10484-015-9309-6

Neurofeedback in Learning Disabled Children: Visual versus Auditory Reinforcement Thalıá Fernańdez1 • Jorge Bosch-Bayard1 • Thalıá Harmony1 • Marıá I. Caballero2 Lourdes Dıáz-Comas3 • Lı´dice Galań3 • Josefina Ricardo-Garcell1 • Eduardo Aubert3 • Gloria Otero-Ojeda4

•

Ó Springer Science+Business Media New York 2015

Abstract Children with learning disabilities (LD) frequently 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 maturation, but only the Auditory Group showed behavioral/ cognitive improvements. In conclusion, the auditory reinforcer was more efficacious in reducing the theta/alpha ratio, and it improved the cognitive abilities more than the visual reinforcer.

& Thalıá Fernańdez [email protected] 1

Departamento de Neurobiologıá Conductual y Cognitiva, Instituto de Neurobiologıá, Universidad Nacional Autońoma de Me´xico, Campus Juriquilla, Boulevard Juriquilla 3001, 76230 Juriquilla, Quere´taro, Mexico

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Facultad de Psicologıá, Universidad Autońoma de Quere´taro, Quere´taro 76010, Mexico

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Centro de Neurociencias de Cuba, Avenida 25 y 158, Playa, La Habana, Cuba

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Facultad de Medicina, Universidad Autońoma del Estado de Me´xico, 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 diagnosed 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 classified as ‘‘specific’’ (reading disorder, mathematics disorder, 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 attentional 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; Fernańdez 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: Fernańdez et al. (2003), Becerra et al. (2006) and Fernańdez 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 Balasubramanian (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, Verleger (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; analogously, 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 responsivity 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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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 produces faster cortical activation than visual stimulation (Pain and Hibbs 2007), and (c) children with Reading Disability show abnormal activity during semantic processing 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 Neurobiologıá, Universidad Nacional Autońoma de Me´xico 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 Quere´taro. 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 elementary 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 (Valde´s 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 diagnosis 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 standardized 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’’;


several of them presented problems in attentional processes, 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 computed 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 treatment using as reinforcement an auditory stimulus (Auditory 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 differences 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; Fernańdez 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 children with a lag in EEG maturation.

behavioral changes. Academic achievement was communicated 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 presented 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).

Procedure Interview of Parents 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 recommendations. A final interview with the parents was also conducted in order to obtain their qualitative evaluation of

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 development, 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 interaction, 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 (Valde´s et al. 1990) and the description of the NFB program (Fernańdez 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 electroencephalographer 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 normative data provided by MEDICID IV. Population parameters 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 (Valde´s 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 (Hernańdez 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 deviation of the normative sample of the same age as the subject, respectively. Taking into account that the EEG

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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 presence 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 distribution 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 (Galań et al. 1997). These mass-univariate methods have been employed to determined changes between before and after treatment in each group.


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 pretreatment 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 differences 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 occurred 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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Fig. 1 Means and standard errors of Verbal IQ, Performance IQ, and Total IQ from the WISC-R in the Auditory and the Visual Groups. No significant differences between before and after NFB were observed

in the Visual Group, but the Verbal IQ (p \ 0.01) and Total IQ (p \ 0.05) increased significantly in the Auditory Group

Fig. 2 Means and standard errors of Omissions, Commissions, Average Response Times, and ADHD scores from the TOVA in the Auditory and the Visual Groups. No significant differences between

before and after NFB were observed in the Visual Group, but in the Auditory Group significant decreases of Commissions (p \ 0.01) and ADHD scores (p \ 0.01) were observed

Table 1 EEG significant differences between groups before NFB treatments

AG \ VG

AG [ VG Global p

Significant leads p \ .05

delta

.02

Fp1, Fp2, C3, C4, Cz

alpha

.05

C3, P3, T5, Cz

Global p

Significant leads p \ .05

Absolute power

beta

Fp1, F3, F8, Fz, Cz

Relative power delta

O2, T6

alpha beta

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P3, Pz Cz


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 principal 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 frontotemporal 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 topographic 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 reinforcer; 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

(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; however, 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 cognitive 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

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

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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

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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


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

the treatment; in addition, the maps show delta decreases in the Auditory Group, and beta increases in the Visual Group, after the treatment

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 (Dıáz de Leoń et al. 1988; John et al. 1980; Matousek and Peterseń 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 reorganization produced by this type of treatment. The sensorimotor 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

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 pseudorandom 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 interpret 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

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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 Garcıá, Nelson Pumariega, Hećtor Belmont, Susana Ange´lica Castro-Chavira, Lourdes Lara, Leonor Casanova, ´ lvarez, Marıá Elena Jua´rez, Eneida PorrasBertha Esquivel, Teresa A Kattz, and Efraıń Santiago for technical assistance, Roberto A. PradoAlcala´ 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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