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- MATERIAL AND METHOD
Abstract The aim of this study was to examine the specific aspects of attention, such as selective attention, sustained attention, and short-term memory in children with attention deficit hyperactivity disorder, combined subtype (ADHD-C). A total of 40 children with a diagnosis of ADHD from the 4th edition of the Diagnostic and Statistical Manual, aged 6–11 years old were compared with 40 controls matched for age and gender on a battery of tests. Short-term memory span and attention was measured by Visual Aural Digit Span Test–Revised. Stroop test and the Turkish version of Cancellation Test were used to assess selective and sustained attention, respectively. In order to check for factor structure in two groups on the test scores, principal component analysis was conducted for both groups separately. Relative to the comparison children, children with ADHD showed significant deficits on tests that are related to different aspects of attention. The results are consistent with the theories explaining the biological basis of ADHD by scattered attention networks in the brain, which have reciprocal dynamic interactions. Further comparative studies are needed to elucidate whether the cognitive processes that are known to be assessed by these tests are specific to ADHD.
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- MATERIAL AND METHOD
Different hypotheses have been put forward to explain behavioral disturbances related to cognitive deficits in attention deficit hyperactivity disorder (ADHD). Neuropsychological studies have focused on vigilance and sustained attention, motoric inhibition, executive functions, and memory.1,2 Delay aversion3 and state regulation impairments4 are two alternatives to consider as underlying at least some ADHD cases. Based on clinical and neuropsychological data it has been stated that both the orbitofrontal cortex and dorsolateral prefrontal cortex are functionally disturbed in ADHD.5
Two models explaining attentional processes through parallel information processing have been proposed. In both models the right parietal and cingulate cortex have an important role in spatial attentional processes.6–8 The model proposed by Posner and Petersen7 defines three interconnected nerve networks (executive control network, alerting network, orienting network).9 Swanson et al. evaluates ADHD as a disorder related to these networks.10 It has been emphasized that the controversy regarding the results of neuropsychological studies is semantic rather than substantive. The semantic issue here is believed to be that the term ‘attention’ has to be related to more than one anatomical network among several brain regions. A recent neuroimaging study has demonstrated altered brain mechanism in ADHD associated with all three attentional networks.11
The objective of the present study was to examine children in ADHD with respect to specific aspects of attention, such as selective attention, sustained attention, and short-term memory. Although a specific model of attention has not been adopted here, a battery of tests that is in relation with different aspects of attention was used. Therefore, it is hypothesized that attentional disturbance in ADHD is not limited to oneaspect of attention, but different types of attention deficits need to be considered.
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- MATERIAL AND METHOD
ADHD-C and NC groups differed on the basis of VADS-R, Stroop Test and CT scores (Wilks' λ = 0.504, F [22, 57] = 2.546, P = 0.002; Table 1). It was found that performances of the ADHD group in the visual-oral and visual-written subtests of VADS-R were lower compared to the controls. In contrast, those components that do not have visual input, namely, aural-oral, aural-written, and the combination score of these subtests aural input (AO + AW) were not found to be significantly different in the two subject groups. This indicated that ADHD subjects had more difficulty in expressing material presented in visual modality of both oral and written format compared to normal subjects.
Table 1. Neuropsychological measures, means and standard deviations for two groups (manova)
|Test||Subtest||ADHD-C (N = 40) Mean (SD)||Controls (N = 40) Mean (SD)||F||P|
|VADS-R||Aural-Oral (AO)||4.13 (1.07)||4.48 (0.85)||2.641||0.108|
|Visual-Oral (VO)||3.63 (1.31)||4.60 (0.96)||12.924||0.001|
|Aural-Written (AW)||3.98 (1.64)||4.45 (0.93)||2.534||0.115|
|Visual-Written (VW)||3.78 (1.49)||4.80 (0.94)||13.503||0.000|
|Aural Input (AO + AW)||8.10 (2.31)||8.93 (1.56)||3.488||0.066|
|Visual Input (VO + VW)||7.40 (2.50)||9.35 (1.69)||16.724||0.000|
|Oral Expression (AO + VO)||7.75 (2.06)||9.03 (1.56)||9.736||0.003|
|Written Expression (AW + VW)||7.75 (2.66)||9.25 (1.74)||8.931||0.004|
|INTRA (AO + VW)||7.90 (2.32)||9.28 (1.47)||10.046||0.002|
|INTER (VO + AW)||7.60 (2.64)||9.00 (1.65)||8.097||0.006|
|STROOP||STR/1 Time (s)||20.38 (12.37)||17.88 (14.73)||0.676||0.414|
|STR/2 Time (s)||21.58 (12.00)||17.48 (11.60)||2.413||0.124|
|STR/3 Time (s)||25.88 (8.58)||20.90 (6.36)||8.861||0.004|
|STR/4 Time (s)||38.70 (13.22)||32.50 (9.74)||5.702||0.019|
|STR/5 Time (s)||55.20 (18.90)||43.88 (10.60)||10.922||0.001|
|CT||Correct responses||56.00 (4.57)||57.85 (2.85)||4.712||0.033|
|Organized letters (OL)||Omission errors||4.00 (4.57)||2.15 (2.85)||4.712||0.033|
|Commission errors||0.10 (0.38)||0.03 (0.16)||1.335||0.252|
|Duration (s)||246.38 (116.47)||201.63 (91.46)||3.652||0.060|
|CT||Correct responses||56.28 (5.15)||58.55 (1.50)||7.184||0.009|
|Organized figures (OF)||Omission errors||3.78 (5.14)||1.45 (1.50)||7.550||0.007|
|Commission errors||1.35 (1.64)||0.93 (1.21)||1.741||0.191|
|Duration (s)||211.38 (75.44)||193.03 (64.57)||1.366||0.246|
|CT||Correct responses||56.15 (4.72)||57.85 (2.52)||4.046||0.048|
|Random letters (RL)||Omission errors||3.85 (4.72)||2.15 (2.52)||4.046||0.048|
|Commission errors||0.05 (0.22)||0.00 (0.00)||2.053||0.156|
|Duration (s)||247.65 (90.07)||215.40 (77.05)||2.962||0.089|
|CT||Correct responses||56.10 (4.83)||57.38 (4.34)||1.542||0.218|
|Random figures (RF)||Omission errors||3.90 (4.83)||2.63 (4.34)||1.542||0.218|
|Commission errors||0.93 (2.15)||0.18 (0.38)||4.704||0.033|
|Duration (s)||191.90 (64.40)||155.53 (55.09)||7.869||0.008|
According to the Stroop Test results, lower performance of children with ADHD in all color naming subtests was observed. In contrast, in the reading-only subtests significant differences were nonexistent between the ADHD and control groups. This indicates a higher deficit in ADHD subjects in color-naming and Stroop interference effect in terms of the observed increase in the reaction time and in the errors in incongruent tasks compared to congruent tasks.
Cancellation Test results showed that children with ADHD showed lower reaction speeds and higher omission/commission errors in CT compared to controls in different subtests of CT. In three of the four subtests of CT, namely, Organized Letters, Random Letters and Organized Figures, finding correct responses and omission of targets were significantly different for ADHD and controls. In contrast, commission errors indicating impulsivity and completion time of CT subtests indicating reaction speeds were higher in ADHD subjects in CT Random Figures subtest.
VADS-R, Stroop, and CT scores were subjected to PCA for the NC group. Five factors were extracted with eigenvalues 7.52 through 1.42 and these factors were found to explain 81.79% of the variance.
VADS-R, Stroop, and CT scores were subjected to PCA for the ADHD-C group. Four factors were extracted with eigenvalues 7.87 through 3.35 and these factors were found to explain 68.87% of the variance.
VADS-R subtest scores that assess attention and short-term memory were gathered under the first factor for both the control and study groups.
For the Stroop test, all the reading and color-naming scores were gathered under factor two for the control group, whereas for the ADHD group only reading scores were under factor two. Stroop scores regarding color-naming and interference effect were gathered under a third factor for the ADHD group.
For CT, in terms of the correct responses, it was found that in the normal control group, scanning behavior was differentiated in terms of the pattern of the stimulus (organized/random) and gathered under different factors (factors 4 and 5). In contrast, in the ADHD group there was no differentiation with regard to the stimulus pattern or type.
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- MATERIAL AND METHOD
The processes in the information processing paradigm are being investigated as the core deficit in ADHD and empiric findings aid in the development of different theories. The conceptual basis of these theories lie on overlapping models related to executive functions, working memory, attention and inhibition.30
In this study it was found that there are deficits in vigilance/sustained attention as well as other attention measures in children with ADHD. These results are consistent with the theories explaining the biological basis of ADHD by scattered attention networks in the brain, which have reciprocal dynamic interactions. These tests are connected with executive functioning such as response organization and working memory, functions which are related to attention.
An important finding in this study is the low performances of the ADHD group in the visual-oral and visual-written subtests of VADS-R. In these subtests, the subject is expected to memorize a set of visually presented number sequences and then give the responses in writing. In this formation that requires monitoring, there is an analogy between a digit span test and working memory. This result shows a parallel structure with previous results comparing memory capacity through digit span.31–33 The lower performance of subjects with ADHD in attention and memory test is taken as a dysfunction related to working memory.30,31 A recent meta-analysis has shown that there are deficits in many of the components of the working memories of ADHD children, regardless from learning disorder and IQ.34
VADS-R assesses short-term memory span, sequencing and motor integration. It is also a serial learning task that necessitates temporal ordering. Serial ordering and sequencing are frontal lobe functions.35,36 Fuster37 has pointed out that temporal ordering which is important in terms of learning and memory is a function of the dorsolateral prefrontal cortex. Studies have also shown the important role of fronto-striatal dopaminergic circuit in working memory.38 Serial learning also comprises proactive interference. Orbitofrontal cortex is related to resistance to interference, therefore, closely related to serial learning.39 The dysfunction of these circuits in ADHD has been shown through neuroimaging studies.40,41
The ADHD children were impaired in the visual modality of the VADS-R in this study, which is like Penney's separate-streams model of short-term verbal memory.42 According to this model, verbal information presented in aural and visual modalities are processed in separate channels with different characteristics and capacities. Aural stimuli elapse into phonological formats much more automatically. In contrast, visual stimuli necessitate a transformation in order to elapse into phonological formats. Clinical studies show that the visual system gains its full function later developmentally and that it is more sensitive to brain damage.43 Electrophysiological and neuroimaging studies also show that there are quantitative differences in activation patterns of the brain in visual and aural verbal working memory tasks without performance differences.44,45 Therefore, it can be concluded that the lower performance of the visual short-term memory, which requires more attentional functions and neuronal capacity, of ADHD children is related to insufficient attentional functions. This result brings on inferences related to psycho-education. It might be reasonable to increase ADHD children's learning abilities through visual materials that are reduced in cognitive content by dividing materials into simple pieces and supporting these by speech-based instructions.
In a neuro-imaging study in which the Stroop effect was investigated in normal adults, all brain regions that showed activation were shown to have functional links with the anterior cingulate (AC).46 Based on these results, the role of AC on attention networks and executive functions such as conflict resolution and impulse control has been pronounced. These neural networks, especially the frontal cortex, are brain regions believed to have an important role in the pathology in ADHD.47 In this study, the lower performance of children with ADHD in all color naming subtests, which is less automatic than reading and requires more attention, is in favor of attentional-executive dysfunction.
In a recent meta-analysis in which children with ADHD were assessed in terms of interference with the standard Stroop Color-Word Task, it was found that there was a higher and more homogenous effect in word reading and color naming, whereas there was a lower effect in interference score.48 It was also found that children with ADHD showed a lower performance in all the Stroop scores.48
Cancellation tests assess vigilance, visual search and speed of response. Ability to attend to visual stimuli based on their spatial locations requires the parietal cortex.26 These tests, which assess selective and sustained attention in children, also have properties such as memorizing the target and learning, using strategies, giving planned responses and the continuance of the behavioral formation that include executive function properties.49
Clinical research to use cancellation tests under time pressure has shown both positive and negative results in terms of differentiating patient groups from controls.49–51 There have been significant differences in terms of completion time, omission and commission errors between controls and ADHD children.52 In this study, it was found that children with ADHD showed lower reaction speeds and higher omission/commission errors in CT. These results are important, because CT results suggested that there are sustained attention deficits related to parietal attention networks as well as dysfunctions in the frontal attention network structures which are shown by the first two tests.
PCA of test scores from these two groups yielded different results: The controls showed a coherent factor structure compared to that of the ADHD group. When evaluated in terms of the correct responses, it was found that in the normal control group, scanning behavior was differentiated in terms of the pattern of the stimulus (organized/random) and gathered under different factors (factors 4 and 5). In contrast, in the ADHD group there was no differentiation with regard to the stimulus pattern or type. This result also shows that there are focused and sustained attentional deficits in ADHD.
The current findings must also be interpreted in light of certain limitations. This study is cross-sectional and conducted with subjects of ADHD-C subtype. Therefore, results may not be true for all ADHD subtypes. In contrast, the strong part of this study is the usage of standardized tests with normative data that have previously been studied in a large population of Turkish children.
To sum up the current results, the battery of tests in this study did have a discriminating power; abnormal scores on the tests were suggestive of ADHD diagnosis. Further comparative studies with other psychiatric disorders are necessary to find out whether the cognitive processes that are known to be assessed by these tests are specific to ADHD.