Characterization of Neuropsychological Functioning in Children with Clinical Features of ADHD

Abstract

Attention deficit with/without hyperactivity is one of the most controversial and currently studied disorders. From a neuropsychological point of view, its characterization is gaining ground with a view to obtaining a more effective diagnosis and treatment. However, there are not many studies that have compared the different profiles of ADHD from this approach. Thus, the aim of the present study was to compare groups of school-aged children with characteristics of attention deficit, hyperactivity-impulsivity and controls, with respect to the neuropsychological variables: saccadic movements, auditory discrimination, executive functions and working memory. A sample of 36 students aged 8-10 years was evaluated, distributed equally among the 3 groups. After analyzing the results obtained from the application of different tests: King-Devick,(KD), Phoneme Articulation Test (PAF), Stroop Color and Word Test and the index of working memory of the Weschler Intelligence Scale for children; it was confirmed that subjects with behavioral characteristics of attention deficit and hyperactivity showed a worse performance than the control group in all variables, and no statistically significant differences were found between inattentive and hyperactive ADHD profiles. Results were discussed and it is concluded that based on the present comparative study, a differential neuropsychological profile cannot be established between children with a characteristic pattern of inattention versus one of hyperactivity-impulsivity, and generally the children with clinical features of ADHD presented a decrease in the neuropsychological variables evaluated.

Keywords: Auditory DiscriminationClinical Features of ADHDExecutive FunctionsNeuropsychological ProfileSaccadic MovementsWorking Memory

Introduction

Attention deficit with and without hyperactivity has been of great interest to neuropsychological and clinical research. It is of high prevalence in the child population and social relevance it has, since it is a condition that continues until adolescence and in some cases until adulthood, causing functional alterations in the individual (APA., 2013) with the consequent emotional impact for those who suffer it. Since the fifth edition of the Diagnostic and Statistical Manual of Mental Disorders (APA., 2014), ADHD has been included among the disorders of neurodevelopment and not among behavioral disorders as before, which consequently accentuates its chronicity (Isorna, 2016).

From the neurobiological viewpoint, attention is a complex process involving various cortical and subcortical structures that participate from sensory integration of stimuli, allowing selective attention, to the inhibitory control of responses and the ability to ignore other stimuli to maintain attentional focus, among others. At school age, normally between 7 and 11-12 years of age, children must have mastered basic movement patterns, improve comprehension and expression through reading and writing, acquire basic instrumental techniques such as reading, writing and calculating with increasing skill and thinking becomes more complex. Therefore, attentional failures that interfere with information processing and behaviour are already evident.

Among the factors involved, saccadic movements are a measure of visual functionality that primarily influence reading, so deficits in ocular motor skills are at the base of many reading difficulties (Miguel, 2017). On the other hand, auditory discrimination of speech sounds, hinders the learning process and can lead to school failure, according to Portellano 2005, quoted in (García-Castellón & Gamazo, 2015).

Each subtype of ADHD has behavioral characteristics that are particularly noticeable in the educational setting, for example, children who exhibit inattentive behaviors may go unnoticed in their classroom, are often identified by the product of their work: noncompliance with tasks, disorder in materials, poorly presented notebooks, etc. On the other hand, children with hyperactivity or impulsivity are quickly detectable through direct observation, their restlessness and impulsivity often lead to friction with their peers or more notorious behavior problems, their execution of tasks is usually quick to the detriment of quality and they may skip test instructions or interpret questions quickly and incorrectly (Abad-Mas et al., 2013).

These behavioral manifestations, if not addressed early, can develop significant learning problems (Aguilera et al., 2014), as well as conflicts between peers, since in adolescence and adulthood the most prevalent symptom is impulsivity, which can be associated with more complicated situations such as substance use and antisocial behavior (APA., 2013).

Among the neuropsychological variables related to attention/hyperactivity, mainly executive functions have been studied (Gaitán & Rey-Anacona, 2013; Romero-Ayuso et al., 2006), and sensory functioning (García & Vergara, 2015), especially visual and auditory, as well as working memory (Dean, 2006).

In an investigation of executive functions in relation to ADHD subtypes, they found that subjects with ADHD-inattentive subtype and ADHD-subtype combined showed significant differences in verbal working memory and persistent errors in categorical fluency. They found no significant differences between the ADHD subtypes in inhibition, set switching, verbal fluency, cognitive flexibility and planning, but they did find significant differences in each of the verbal working memory tasks. Also, the ADHD-comorbid group with ODT or CT reached more severe levels of executive functions impairment, without finding differences between the inattentive group and the control group in such executive functions (Saydam et al., 2015). In other research, it was found that the combined subtype of ADHD had generalized deficiencies while the attempt had a lower performance in working memory and planning tasks, but not in all the executive functions evaluated (Romero-Ayuso et al., 2006).

According to Aguilera et al. (2014), ADHD is associated with learning disabilities: with dyslexia in 39% of cases, with dysgraphia in 60% and dyscalculia in 26% of cases. In turn, sensory maturation problems affect the processing of information making it ineffective (López Juez, 2010), therefore, affect the attention process and consequently learning. In the line of sensory research, (Torcal, 2012) found associations between saccadic movements and difficulties in reading speed and comprehension in the first grades of primary school. On the other hand, links have been reported between a history of otitis media and hyperactive and inattentive behaviors in school children (Adesman et al., 1990) and signs of dysfunctional auditory processing through electrophysiological assessments, findings that seem to reaffirm the incidence of sensory processing on inattentive and hyperactive-impulsive behaviors of ADHD.

García and Vergara (2015) found significant differences in saccadic movements and auditory phoneme discrimination, but not in laterality of children with and without ADHD between 7 and 11 years. They emphasize the importance of working with different information processing systems for the maturation of the central nervous system as a whole.

The importance of working memory in relation to ADHD has also been investigated. In a study on the detection of cognitive profiles using the WISC-IV (Fenollar-Cortés et al., 2015), significant differences were found in the indices of working memory and processing speed between the clinical subgroups of ADHD, with the index of processing speed being clearly lower than that of working memory in the inattentive group and vice versa, the combined subgroup obtained lower scores in working memory than in processing speed. They found no difference between the other indices, so verbal comprehension and perceptual reasoning were not affected by belonging to one or another subtype of AD-H.

Although there is a lot of research that relates learning and neuropsychological variables to ADHD (Aguilera et al., 2014; Martín-González et al., 2008), few establish differentiations by profile or clinical subgroups of the disorder (Filippetti & Mías, 2009), evaluating rather groups with the presence of the disorder as a whole -without differentiating subtype- versus control groups, and a precise neuropsychological characterization of this disorder has not been achieved.

Problem Statement

The problem posed in the present study is to discern the specific neuropsychological characteristics of each diagnostic subtype of ADHD on the basis of some criteria for comparison between them. This raises the question of what the specific neuropsychological substrate for each subtype of ADHD is, with the interest of helping to refine the detection, diagnosis and effective treatment for this problem. Specifically, we want to compare the variables of visual functioning through saccadic movements, auditory functioning through auditory phoneme discrimination, working memory and executive functions through Stroop-type tasks, in primary school children with behavioural characteristics of ADHD inattentive and hyperactive-impulsive subtype in contrast with a control group, and to discern whether there are specific neuropsychological characteristics of each of these groups.

Research Questions

How is the visual, auditory, executive functions and working memory functioning in primary school children with an inattentive versus a hyperactive/impulsive profile?

Purpose of the Study

Specifically, the following research objectives are proposed:

Research Methods

For the selection of the groups, Barkley's Disruptive Behavior Evaluation Scale (EECP) for parents and teachers created in 1997 was administered to all 4th, 5th, and 6th grade students on campus. This scale is based on DSM-5 criterion A for ADHD, which was considered for this study. The instrument alternates items of inattention with items of hyperactivity-impulsivity, which are scored from "0" (never) to "3" (almost always), with the possible range of scores being from "0" to "54" points. The internal consistency of the instrument is strong, with a Crombach alpha coefficient of 0.85 to 0.92 for all ages (Moreno & Martínez, 2010). Based on the results provided by both groups of informants, students who met criteria for inattention and hyperactivity-impulsivity (both informants had to agree on this to be considered) were selected to be part of the experimental groups (Table 1 shows the scores obtained in the predominant scale, inattention or hyperactivity) and those who did not meet them and scored in the lower end of the scale were part of the control group. Those subjects who scored on both profiles, which would correspond to the "combined" subtype, which was not considered in this study.

The King-Devick Test was used to measure saccadic movements (King, 1976). The test consists of reading sequences of numbers, first on a test plate, then the numbers are arranged with arrows indicating eye tracking, a second plate without the tracking marks, and the last plate with the numbers spaced further apart and without many visual references, which should also be read as if it were text. The reading time is measured, and the errors made are counted in order to be contrasted with the scales that exist by age from 6 to 14 years (Olivera-Plaza, 2015).

To measure auditory discrimination, we used the Phoneme Auditory Discrimination Test (PAF), developed by Vallés in 1990, which consists of reading a list of 28 items made up of syllables and words that the subject must repeat, placing the subject with their back to the examiner. This is important to avoid lip reading. From the age of 6, the presence of failures in the test suggests difficulties in auditory discrimination (García & Vergara 2015).

To measure executive functions, the Stroop Color and Word Test (Golden, 1994), which measures response inhibition (one of the components of executive functions), is used as an instrument. It throws a measure of the interference between two instructions that compete in the brain to emit a response. One of them elicits an automatic response, which consists of reading words and the other requires more selective attention and cognitive control to achieve the objective of the task. It is to nominate the color of the ink in which the word is written, being incongruent with the content of the word. For example, the word "blue" is written in red ink and the correct response is to read "red" instead of "blue". The Spanish version of Golden 2001 was used, consisting of three plates, each with 100 items. For each sheet, the subject has 45 seconds to answer as many items as possible in that time. On sheet one, Words (P), the words red, green and blue, written in black ink in columns to be read aloud, are presented. On the second sheet, Colors (C), groups of X's (XXXX) written in red, green and blue are presented, randomly arranged in 5 columns of 20 items each, and without two continuous colors being repeated. Finally, sheet three, of Word-Color (PC), is formed by the words on sheet one written in the colors of sheet two, the word always being incongruent with the color of the ink, and the subject is asked to mention the color in which the word is written, thus inhibiting the reading of its graphemes.

In the test score, the answers given to each sheet are counted and additionally the interference index is calculated based on the formula established in the manual. The higher the value, the better control the subject has over the interference, and it is an indicator of cognitive flexibility. People who have a score greater than zero have a high resistance to interference (Golden, 1994). By contrast, the lower the rate of interference, the less inhibitory control of the response.

Finally, the operating memory index of the Intelligence Scale for children (Wechsler, 2005) was used as a measure of working memory. It is obtained based on the scalar scores obtained in two subtests, which are Digit Retention and Letters and Numbers, each with age rules. The scalar score of each subtest has an average of 10 and standard deviation of 3, while the operating memory index (OMI), like the other composite scores obtained in the WISC-IV, has an average of 100 and standard deviation of 15 (Wechsler, 2005).

In table 2 , the neuropsychological instruments used and their form of interpretation are summarized:

Findings

A descriptive analysis was conducted based on the mean and standard deviation of the quantitative variables (age and each of the study measures), as well as their response ranges (minimum and maximum); these data are summarized in Table 3 :

Based on the descriptive statistics, there is a tendency to achieve better results in the control group than in the ADHD groups. On the other hand, between the Inattentive and Hyperactive groups a different behaviour is observed according to the study variable, for example, in the saccadic movements there is a greater time and number of errors in the H-I group than in the Inattentive group, which suggests greater deficiencies in the visual functionality of hyperactive children than inattentive ones, probably due to their impulsivity. In the discrimination of phonemes, the study groups obtain the same average, with the Inattentive group being more homogeneous than the H-I; in the executive functions, a tendency to have greater interference is observed in the H-I children and the working memory tends to be slightly lower in the Inattentive children.

Inferential statistics were also used to compare groups in the research variables as follows: for the comparison of the groups (Inattentive/Hyperactive-Impulsive/Control), the non-parametric Kruskal-Wallis test was applied, as they were three independent groups, with a sample size of less than 30, a categorical independent variable with three categories (Inattentive, Hyperactive-Impulsive and Controls) and quantitative dependent variables (Saccadic movements, auditory discrimination, executive functions and working memory). Tests were performed for each variable to compare between the three groups, using the SPSS v.25 program, considering significant the results with a p value equal to or less than 0.05.

The results of the statistical tests are compiled below:

Conclusion

It is concluded that, in the different study variables, the control group showed a better performance than the Inattentive and the Hyperactive-Impulsive, reaching notably different results. This coincides with the findings of García et al. (2014), and García and Vergara (2015), who found deficiencies in saccadic movements and auditory discrimination in school-aged children with ADHD, and with Fenollar-Cortés et al. (2015), who found deficits in working memory and processing speed in children with Inattention. Also, Morales-Avendaño and Meneses-Ortega (2003) found that children with ADHD showed alterations in the ability to focus and maintain attention, as well as failures in FFEE.

In none of the variables of the study were found statistically significant differences between the groups of Inattention and Hyperactive-Impulsive, although descriptively a certain differential tendency can be appreciated. Therefore, it is concluded that neuropsychological functioning in primary school children with ADHD is diminished compared to children without ADHD, but it is not possible to establish a differential neuropsychological profile between inattention and hyperactivity-impulsivity profiles based on the variables studied.

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