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Working memory functioning in children with attention-deficit/ hyperactivity disorder (ADHD): A comparison between subtypes and normal controls Kate Cockcroft
a
a
Department of Psychology, School of Human and Community Development , University of the Witwatersrand , PO WITS 2050, Johannesburg, South Africa Published online: 19 Dec 2011.
To cite this article: Kate Cockcroft (2011) Working memory functioning in children with attention-deficit/hyperactivity disorder (ADHD): A comparison between subtypes and normal controls, Journal of Child & Adolescent Mental Health, 23:2, 107-118, DOI: 10.2989/17280583.2011.634545 To link to this article: http://dx.doi.org/10.2989/17280583.2011.634545
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [California Poly Pomona University] at 15:38 02 November 2014
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/ terms-and-conditions
Journal of Child and Adolescent Mental Health 2011, 23(2): 107–118 Printed in South Africa — All rights reserved
Copyright © NISC Pty Ltd
JOURNAL OF CHILD AND ADOLESCENT MENTAL HEALTH ISSN 1728–0583 EISSN 1728–0591 DOI: 10.2989/17280583.2011.634545
Research Paper
Downloaded by [California Poly Pomona University] at 15:38 02 November 2014
Working memory functioning in children with attentiondeficit/hyperactivity disorder (ADHD): A comparison between subtypes and normal controls Kate Cockcroft Department of Psychology, School of Human and Community Development, University of the Witwatersrand, PO WITS 2050, Johannesburg, South Africa Email: [email protected] Objective: Children with attention-deficit/hyperactivity disorder (ADHD) often experience working memory difficulties. However, research findings are inconsistent, making it difficult to compare results across studies. There are several reasons for this inconsistency. Firstly, most studies make no distinction between ADHD subtypes, despite evidence that predominantly inattentive ADHD (ADHD/I) represents a different neurocognitive profile to the hyperactive-impulsive subtype (ADHD/HI). Secondly, documented studies use different tests of working memory which may be measuring different skills. Some assess only the verbal components of working memory and others the visuo-spatial; few of the tests assess both. Further, some tests employ a recognition methodology and others use recall, which require different brain regions and cognitive processes. To clarify these inconsistencies, the verbal and visuo-spatial working memory of children with ADHD/I, ADHD/HI and a control group with no ADHD symptoms were compared. Method: The Automated Working Memory Assessment and Ravens Coloured Progressive Matrices were administered to 72 children (ADHD/I n = 27; ADHD/HI n = 25; control n = 20). Results: The ADHD groups performed similarly, but were significantly poorer than the control group in all aspects of working memory. Storage abilities were stronger than processing abilities, while verbal and visuo-spatial abilities were equally developed for all groups. Conclusion: ADHD-related deficits were apparent across working memory components, even when IQ was controlled for, suggesting a generalised impairment.
Introduction Controversy about the validity of attention deficit/hyperactivity disorder (ADHD) and concerns about the rapid increase in its prevalence, have led researchers to attempt to formulate a single theory of the disorder. Some have suggested that it could be useful to identify endophenotypes or measurable cognitive characteristics that underlie and predict manifest behaviour (e.g. Castellanos and Tannock 2002). Deficits in working memory, which would have an impact on the ability to maintain and foreground specific information and simultaneously reduce distractions from irrelevant stimuli, have been proposed as an endophenotype involved in the expression of ADHD difficulties (Barkley 1997, Castellanos and Tannock 2002). However, there is uncertainty whether working memory deficits play a central or peripheral role in the phenotypic expression of ADHD. Several researchers suggest that working memory deficits are one of many executive functions that are undermined in children with ADHD by poorly regulated/ underdeveloped behavioural inhibition control processes that fail to inhibit processing of a response Journal of Child & Adolescent Mental Health is co-published by NISC (Pty) Ltd and Routledge, Taylor & Francis Group
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to irrelevant stimuli (e.g. Hasher and Zacks 1988, Barkley 1997, Quay 1997, Sonuga-Barke 2003, Willcutt et al. 2005, Barkley and Murphy 2006, Engel, Santos and Gathercole 2008). For example, Barkley (1997) maintains that the primary deficit in ADHD/HI is the difficulty inhibiting behaviour, and that all other symptoms characteristic of ADHD/HI are secondary to this reduced capacity. It is, however, also possible that working memory deficits may be a core component or endophenotype in children with ADHD that results in poor behavioural inhibition. Uncovering the directional nature of the relationship is difficult, if not impossible. Nonetheless, it would be valuable to explore whether working memory deficits are generalised across verbal and visuo-spatial aspects of working memory in children with ADHD. This would indicate whether the difficulties with behavioural inhibition are specific to one or both working memory modalities. Thus, the primary aim of the study reported here was to compare the verbal and visuo-spatial working memory of children with ADHD to that of children without any ADHD symptoms. The theoretical framework for this investigation was Baddeley and Hitch’s (1974) working memory model, which is supported by extensive neuropsychological (Baddeley 2003), neuroanatomical (Smith, Jonides and Koeppe 1996), neuroimaging (Fassbender and Schweitzer 2006) and factor analytic (Alloway, Gathercole and Pickering 2006) investigations. Based on this model, distinctions are made between the passive, storage aspects of working memory, as embodied by the phonological loop and the visuo-spatial sketchpad (previously referred to as short-term memory), and the more active, planning and processing aspects, as represented by the central executive. The short-term storage components of working memory are usually assessed using simple memory span tasks (e.g. digit, word or visuo-spatial span tasks) and the processing components of working memory are typically assessed with complex memory span tasks, which require ongoing manipulation and storage of information during presentation, followed by sequential recall (e.g. sentence reading and recall span tasks). For simplicity (and to follow existing conventions), tasks requiring simple storage with no explicit concurrent processing are referred to here as short-term memory (STM) tasks and complex span tasks that include both a storage and processing component, as complex working memory (WM) tasks. Working memory in children with attention-deficit/hyperactivity disorder The importance of working memory in learning, language and reasoning has been well documented and there is considerable evidence to indicate that working memory capacity constrains children’s academic achievement (Gathercole and Pickering 2000, Baddeley 2003, Gathercole and Pickering 2003, Alloway 2009). In fact, working memory ability at the start of formal education is a more powerful predictor of subsequent academic success than IQ, such that Alloway (2008) dubbed it “the new IQ”. This addresses concerns that general intelligence is not a reliable predictor of academic success, since individuals with average and higher IQ scores, particularly those diagnosed with ADHD, may perform poorly on learning outcomes. An important difference between working memory and IQ is that the former is relatively uninfluenced by environmental factors, such as the quality of social and intellectual input in the home environment, as well as socio-economic status and preschool education (Alloway et al. 2004, Engel et al. 2008). In contrast, IQ assessments measure knowledge that the child has already learned and are partly influenced by the child’s home background and access to resources. Thus, working memory appears to be a relatively “pure” measure of a child’s learning potential. Substantial research has been conducted on the neurophysiological substrates that underlie working memory function. The prefrontal cortex appears to be the most important of these and coincides with those substrates known to be affected in children with ADHD. Further, working memory function is dependent on dopamine, which is consistent with the association between ADHD and atypical dopaminergic transmission (Cook et al. 1995, Williams and Goldman-Rakic 1995). Drugs that ameliorate the symptoms of ADHD, such as methylphenidate and amphetamine, are those that facilitate dopaminergic transmission (Volkow et al. 1995) and also improve working memory. Thus, since many classroom activities place heavy demands on working memory, children who have deficits in this area would be unable to deal with these demands and fail to acquire the knowledge and skills necessary for competence in important academic areas such as literacy
Downloaded by [California Poly Pomona University] at 15:38 02 November 2014
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and mathematics. Since the neurophysiological substrates involved in optimal working memory functioning are those that appear to be impaired in children with ADHD, this adds further support for the idea that working memory function may be a key area of difficulty in this population. Despite the obvious connections, cognitive studies of working memory deficits in children with ADHD have yielded inconsistent results, making it difficult to draw firm conclusions from them. There are several possible reasons for this. Firstly, the reported studies use a wide range of working memory measures, which may be measuring different cognitive abilities. For example, the use of recall or recognition memory tasks may account for differences in findings as they require different cognitive processes and are associated with different anatomical brain sites. Recall tasks involve the dorsolateral prefrontal cortex and place greater demands on active maintenance of stimuli and internally generated mnemonic strategies than recognition tasks which implicate the ventromedial prefrontal cortex (Cabeza et al. 1997, Baddeley et al. 1999). Consequently, this study used only recall tests and attempted to compare results to studies that employed similar measures of working memory. A second difficulty in drawing comparisons across published studies is that many do not report co-morbidity rates or differentiate between ADHD subtypes in their samples, despite the distinctly different neurocognitive profiles (Barkley, DuPaul and McMurray 1990; Milich, Balentine and Lynam 2001). The existence of the different subtypes of ADHD and their classification is the subject of some controversy. Currently, the International Statistical Classification of Diseases and Related Health Problems (ICD-10) gives a more constrained description of the ADHD subtypes than the Diagnostic and Statistical Manual of Mental Disorders (fourth edition, DSM-IV-TR) and does not recognise the DSM-IV predominantly inattentive subtype. The DSM-IV-TR subdivision of ADHD into three categories (i.e. predominantly inattentive, hyperactive-impulsive and combined subtype) is based on evidence from factor analytic studies that have consistently yielded two factor solutions that differentiate symptoms of hyperactivity-impulsivity from symptoms of inattention (Lahey, Carlson and Frick 1997). Barkley (1997) also explicitly distinguishes between ADHD/I and ADHD/ HI subtypes in his behavioural inhibition model, stating that the difficulty inhibiting behaviour refers only to the Combined and ADHD/HI subtypes. He argues that the primary impairment of the ADHD/I subtype is inattention, rather than problems with inhibition of responses. Thus, there appears to be support for the existence of the two subtypes which suggests that studies that combine these samples are problematic and the conclusions drawn from them may be flawed. Consequently, this study compared working memory performance in children diagnosed with the two distinct ADHD subtypes and also compared these abilities to those of children without ADHD. Despite the inconsistencies in the literature in the area, it is necessary to provide a brief review of the predominant findings against which the results of this study can be evaluated. Two relatively recent meta-analytic reviews provide confirmatory evidence of working memory deficits in children with ADHD relative to controls, even after controlling for co-morbid learning and language disorders, intelligence and reading achievement (Martinussen et al. 2005, Willcutt et al. 2005). Many studies report normal STM verbal storage (most commonly assessed with the Digits Forwards task) in children with ADHD (Lazar and Frank 1998, Williams et al. 2000, Rucklidge and Tannock 2002). However, when assessed on the Digits Backwards task (verbal STM storage plus complex processing), these children perform significantly worse than controls (McInnes et al. 2003). This suggests that passive span is not affected in children with ADHD, as Forward Digit Span makes demands primarily on the phonological loop and articulatory rehearsal processes, while Digits Backwards draws on these processes as well as on the central executive. There are considerably fewer studies that have investigated visuo-spatial working memory in children with ADHD. Visual span tasks are a visual analogue to the Digits Forwards task and require the child to reproduce a sequence of locations on a display demonstrated first by the researcher. Such tests are generally used to assess passive visuo-spatial storage in working memory. Significantly lower performance has been found on such tasks by children with ADHD compared to controls (Kempton et al. 1999, Williams et al. 2000, Barnett et al. 2001, Tripp, Ryan and Pearce 2002, McInnes et al. 2003). However, of the reported studies, many did not control for IQ differences between the ADHD and control groups (e.g. Tripp et al. 2002, McInnes et al. 2003)
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or included samples that had not been formally diagnosed with ADHD (e.g. Williams et al. 2000). In the two studies where ADHD and control groups were matched for IQ and age (e.g. Kempton et al. 1999, Barnett et al. 2001), spatial span deficits were still evident, suggesting deficits in visuo-spatial STM in children with ADHD. Given the impairment in central executive functioning predicted by many theories of ADHD, it is surprising that there is minimal literature on complex span tasks that evaluate these aspects of working memory in this population. Three studies demonstrate no impairment in children with ADHD relative to controls matched for IQ on such tasks (Siegel and Ryan 1989, Kunsti, Oosterlaan and Stevenson 2001, Willcutt, Pennington and Boada 2001). The only exception to this pattern is a study by Cohen et al. (2000), who found that children with ADHD performed below the normative mean on such tasks, but were not significantly different from a control group of children with other psychological disorders. The complex span tasks used in these studies focused on the verbal processing components of working memory. None of the reviewed studies drew comparisons between the different subtypes of ADHD in their samples and only 30% reported subtype ratios. Thus, the review of documented studies shows that there appears to be evidence for a deficit in non-verbal/visuo-spatial STM tasks but not in verbal STM tasks, while complex verbal working memory does not appear to be impaired. However, these findings may be related the age of the sample, since Westerberg et al. (2004) found that a test of visuo-spatial working memory (STM and complex processing combined) discriminated between older children and adolescents (aged 12–15 years) with ADHD and controls, but not between younger children (aged 7.5–11.5 years). This suggests that complex visuo-spatial working memory may not be impaired in young children with ADHD and may be a sensitive measure of cognitive deficits in older children with the disorder. Thus, the issue is complicated by developmental differences in working memory. Developmental studies suggest a fundamental transformation in children’s use of working memory, changing from primarily visual encoding before school entry to a combined visual-verbal strategy within the first years of formal schooling, to finally the adult-like reliance on the verbal subsystem (Palmer 2000, Pickering 2001). Consequently, it would be useful to investigate whether children with ADHD/I and ADHD/HI demonstrate the typical pattern of working memory development. Aims of the study This study was novel in its attempt to compare the performance of children with predominantly inattentive (ADHD/I) and predominantly hyperactive/impulsive (ADHD/HI) ADHD and a control group without any symptoms of ADHD on both verbal and non-verbal working memory tasks. The aim was to address the following questions: 1. Do the ADHD groups have deficits in verbal or spatial working memory? It was anticipated that the children with ADHD would show impaired performance relative to the controls on non-verbal STM, but not on verbal STM, nor on any aspects of complex working memory processing. 2. Do children with the different subtypes of ADHD have differential deficits on verbal versus spatial working memory tasks? It was anticipated that they would be equally impaired in both tasks, suggesting a generalised impairment in working memory. 3. Do children with the different subtypes of ADHD show similar profiles of strength and weakness in the various aspects of working memory (storage versus processing and verbal versus non-verbal) than controls? It was anticipated that they would be better at storage as opposed to processing and at visuo-spatial as opposed to verbal tasks, as is the pattern in typically developing children of this age. Method A between-subjects ex post facto research design was used to investigate whether there were differences in the working memory of children diagnosed with ADHD, predominantly inattentive subtype and ADHD, predominantly hyperactive/impulsive subtype and a control group of children with no symptoms of ADHD.
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Participants There were three groups of participants: ADHD/I (n = 27), ADHD/HI (n = 25) and a comparison group (n = 20). They were aged between 6.6–11.25 years. As shown in Table 1, there were no significant group differences in terms of age. The children with ADHD were recruited from four special education schools and were matched exactly for grade, gender and ethnicity, and within six months for age, to a control group of children recruited from three mainstream primary schools. The participants came from middle to upper socio-economic backgrounds and their home language and language of tuition was English. Inclusion criteria for the ADHD groups: These children had all been diagnosed with one of the subtypes of ADHD by their respective school psychologists using the DSM-IV-TR (APA 1994) criteria, the Conners’ Rating Scale-Revised (CRS-R) (Conners et al. 1998a) and the Wechsler Intelligence Scale for Children (Fourth Edition) (WISC-IV), as part of the criteria for entry to the remedial schools. Children were included in the study if their Full Scale IQ on the WISC-IV was in the average range (1Q > 85) and they met the Conner’s and DSM criteria for diagnosis. As shown in Table 1, there were no significant differences between the Full Scale WISC-IV scores of the two ADHD groups. The children were requested not to take their ADHD medication for 24 hours before testing. Only those children whose parents agreed to this could be included. This was an important requirement as psycho-stimulant medication may affect visuo-spatial working memory performance (Sinha, Sagar and Mehta 2008). Participants whose parents agreed to this condition brought their medication with them to school and took it after the tests were complete. Exclusion criteria for the ADHD groups: Children with co-morbid anxiety disorders, sensory, motor or neurological impairment, seizure disorders, psychosis, pervasive developmental disorder or mood disorder were excluded from this study. For this reason fewer than 50% of the sample had co-morbid disorders. As shown in Table 1, the ADHD/HI group had significantly more co-morbid disorders than the ADHD/I group. Inclusion criteria for the comparison group: The children in the control group were all assessed for absence of ADHD symptomatology using the DSM-IV-TR (APA 1994) criteria and the Conners’ Rating Scale- Revised (Conners et al. 1998a). In addition, they were screened for the absence of behavioural problems on the Conners’ Parent and Teacher Rating Scales-Revised (Conners et al. 1998b). Specifically, these children had to exhibit fewer than six symptoms of inattention and fewer than six symptoms of hyperactivity-impulsivity, as rated by parents and teachers on the
Table 1: Descriptive characteristics of matched groups of children with ADHD and control group
Variable Age Gender (male/female) WISC IV
ADHD/I (n = 27) Mean SD 9.1 2.89 18/9 92
ADHD/HI (n = 25) Mean SD 9.3 3.75 15/10
10.09
93
Control (n =20) Mean SD 8.54 2.3 10/10
13.54
Comorbidity rates ODD CD LD
0 4 0
4 1 5
0 0 0
DCD
0
1
0
F 1.32 p = 0.07 0.07a p = 0.10 2.3 p = 0.07 9.97a * p = 0.03
*p F
Journal of Child & Adolescent Mental Health Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/rcmh20
Working memory functioning in children with attention-deficit/ hyperactivity disorder (ADHD): A comparison between subtypes and normal controls Kate Cockcroft
a
a
Department of Psychology, School of Human and Community Development , University of the Witwatersrand , PO WITS 2050, Johannesburg, South Africa Published online: 19 Dec 2011.
To cite this article: Kate Cockcroft (2011) Working memory functioning in children with attention-deficit/hyperactivity disorder (ADHD): A comparison between subtypes and normal controls, Journal of Child & Adolescent Mental Health, 23:2, 107-118, DOI: 10.2989/17280583.2011.634545 To link to this article: http://dx.doi.org/10.2989/17280583.2011.634545
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [California Poly Pomona University] at 15:38 02 November 2014
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/ terms-and-conditions
Journal of Child and Adolescent Mental Health 2011, 23(2): 107–118 Printed in South Africa — All rights reserved
Copyright © NISC Pty Ltd
JOURNAL OF CHILD AND ADOLESCENT MENTAL HEALTH ISSN 1728–0583 EISSN 1728–0591 DOI: 10.2989/17280583.2011.634545
Research Paper
Downloaded by [California Poly Pomona University] at 15:38 02 November 2014
Working memory functioning in children with attentiondeficit/hyperactivity disorder (ADHD): A comparison between subtypes and normal controls Kate Cockcroft Department of Psychology, School of Human and Community Development, University of the Witwatersrand, PO WITS 2050, Johannesburg, South Africa Email: [email protected] Objective: Children with attention-deficit/hyperactivity disorder (ADHD) often experience working memory difficulties. However, research findings are inconsistent, making it difficult to compare results across studies. There are several reasons for this inconsistency. Firstly, most studies make no distinction between ADHD subtypes, despite evidence that predominantly inattentive ADHD (ADHD/I) represents a different neurocognitive profile to the hyperactive-impulsive subtype (ADHD/HI). Secondly, documented studies use different tests of working memory which may be measuring different skills. Some assess only the verbal components of working memory and others the visuo-spatial; few of the tests assess both. Further, some tests employ a recognition methodology and others use recall, which require different brain regions and cognitive processes. To clarify these inconsistencies, the verbal and visuo-spatial working memory of children with ADHD/I, ADHD/HI and a control group with no ADHD symptoms were compared. Method: The Automated Working Memory Assessment and Ravens Coloured Progressive Matrices were administered to 72 children (ADHD/I n = 27; ADHD/HI n = 25; control n = 20). Results: The ADHD groups performed similarly, but were significantly poorer than the control group in all aspects of working memory. Storage abilities were stronger than processing abilities, while verbal and visuo-spatial abilities were equally developed for all groups. Conclusion: ADHD-related deficits were apparent across working memory components, even when IQ was controlled for, suggesting a generalised impairment.
Introduction Controversy about the validity of attention deficit/hyperactivity disorder (ADHD) and concerns about the rapid increase in its prevalence, have led researchers to attempt to formulate a single theory of the disorder. Some have suggested that it could be useful to identify endophenotypes or measurable cognitive characteristics that underlie and predict manifest behaviour (e.g. Castellanos and Tannock 2002). Deficits in working memory, which would have an impact on the ability to maintain and foreground specific information and simultaneously reduce distractions from irrelevant stimuli, have been proposed as an endophenotype involved in the expression of ADHD difficulties (Barkley 1997, Castellanos and Tannock 2002). However, there is uncertainty whether working memory deficits play a central or peripheral role in the phenotypic expression of ADHD. Several researchers suggest that working memory deficits are one of many executive functions that are undermined in children with ADHD by poorly regulated/ underdeveloped behavioural inhibition control processes that fail to inhibit processing of a response Journal of Child & Adolescent Mental Health is co-published by NISC (Pty) Ltd and Routledge, Taylor & Francis Group
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to irrelevant stimuli (e.g. Hasher and Zacks 1988, Barkley 1997, Quay 1997, Sonuga-Barke 2003, Willcutt et al. 2005, Barkley and Murphy 2006, Engel, Santos and Gathercole 2008). For example, Barkley (1997) maintains that the primary deficit in ADHD/HI is the difficulty inhibiting behaviour, and that all other symptoms characteristic of ADHD/HI are secondary to this reduced capacity. It is, however, also possible that working memory deficits may be a core component or endophenotype in children with ADHD that results in poor behavioural inhibition. Uncovering the directional nature of the relationship is difficult, if not impossible. Nonetheless, it would be valuable to explore whether working memory deficits are generalised across verbal and visuo-spatial aspects of working memory in children with ADHD. This would indicate whether the difficulties with behavioural inhibition are specific to one or both working memory modalities. Thus, the primary aim of the study reported here was to compare the verbal and visuo-spatial working memory of children with ADHD to that of children without any ADHD symptoms. The theoretical framework for this investigation was Baddeley and Hitch’s (1974) working memory model, which is supported by extensive neuropsychological (Baddeley 2003), neuroanatomical (Smith, Jonides and Koeppe 1996), neuroimaging (Fassbender and Schweitzer 2006) and factor analytic (Alloway, Gathercole and Pickering 2006) investigations. Based on this model, distinctions are made between the passive, storage aspects of working memory, as embodied by the phonological loop and the visuo-spatial sketchpad (previously referred to as short-term memory), and the more active, planning and processing aspects, as represented by the central executive. The short-term storage components of working memory are usually assessed using simple memory span tasks (e.g. digit, word or visuo-spatial span tasks) and the processing components of working memory are typically assessed with complex memory span tasks, which require ongoing manipulation and storage of information during presentation, followed by sequential recall (e.g. sentence reading and recall span tasks). For simplicity (and to follow existing conventions), tasks requiring simple storage with no explicit concurrent processing are referred to here as short-term memory (STM) tasks and complex span tasks that include both a storage and processing component, as complex working memory (WM) tasks. Working memory in children with attention-deficit/hyperactivity disorder The importance of working memory in learning, language and reasoning has been well documented and there is considerable evidence to indicate that working memory capacity constrains children’s academic achievement (Gathercole and Pickering 2000, Baddeley 2003, Gathercole and Pickering 2003, Alloway 2009). In fact, working memory ability at the start of formal education is a more powerful predictor of subsequent academic success than IQ, such that Alloway (2008) dubbed it “the new IQ”. This addresses concerns that general intelligence is not a reliable predictor of academic success, since individuals with average and higher IQ scores, particularly those diagnosed with ADHD, may perform poorly on learning outcomes. An important difference between working memory and IQ is that the former is relatively uninfluenced by environmental factors, such as the quality of social and intellectual input in the home environment, as well as socio-economic status and preschool education (Alloway et al. 2004, Engel et al. 2008). In contrast, IQ assessments measure knowledge that the child has already learned and are partly influenced by the child’s home background and access to resources. Thus, working memory appears to be a relatively “pure” measure of a child’s learning potential. Substantial research has been conducted on the neurophysiological substrates that underlie working memory function. The prefrontal cortex appears to be the most important of these and coincides with those substrates known to be affected in children with ADHD. Further, working memory function is dependent on dopamine, which is consistent with the association between ADHD and atypical dopaminergic transmission (Cook et al. 1995, Williams and Goldman-Rakic 1995). Drugs that ameliorate the symptoms of ADHD, such as methylphenidate and amphetamine, are those that facilitate dopaminergic transmission (Volkow et al. 1995) and also improve working memory. Thus, since many classroom activities place heavy demands on working memory, children who have deficits in this area would be unable to deal with these demands and fail to acquire the knowledge and skills necessary for competence in important academic areas such as literacy
Downloaded by [California Poly Pomona University] at 15:38 02 November 2014
Journal of Child and Adolescent Mental Health 2011, 23(2): 107–118
109
and mathematics. Since the neurophysiological substrates involved in optimal working memory functioning are those that appear to be impaired in children with ADHD, this adds further support for the idea that working memory function may be a key area of difficulty in this population. Despite the obvious connections, cognitive studies of working memory deficits in children with ADHD have yielded inconsistent results, making it difficult to draw firm conclusions from them. There are several possible reasons for this. Firstly, the reported studies use a wide range of working memory measures, which may be measuring different cognitive abilities. For example, the use of recall or recognition memory tasks may account for differences in findings as they require different cognitive processes and are associated with different anatomical brain sites. Recall tasks involve the dorsolateral prefrontal cortex and place greater demands on active maintenance of stimuli and internally generated mnemonic strategies than recognition tasks which implicate the ventromedial prefrontal cortex (Cabeza et al. 1997, Baddeley et al. 1999). Consequently, this study used only recall tests and attempted to compare results to studies that employed similar measures of working memory. A second difficulty in drawing comparisons across published studies is that many do not report co-morbidity rates or differentiate between ADHD subtypes in their samples, despite the distinctly different neurocognitive profiles (Barkley, DuPaul and McMurray 1990; Milich, Balentine and Lynam 2001). The existence of the different subtypes of ADHD and their classification is the subject of some controversy. Currently, the International Statistical Classification of Diseases and Related Health Problems (ICD-10) gives a more constrained description of the ADHD subtypes than the Diagnostic and Statistical Manual of Mental Disorders (fourth edition, DSM-IV-TR) and does not recognise the DSM-IV predominantly inattentive subtype. The DSM-IV-TR subdivision of ADHD into three categories (i.e. predominantly inattentive, hyperactive-impulsive and combined subtype) is based on evidence from factor analytic studies that have consistently yielded two factor solutions that differentiate symptoms of hyperactivity-impulsivity from symptoms of inattention (Lahey, Carlson and Frick 1997). Barkley (1997) also explicitly distinguishes between ADHD/I and ADHD/ HI subtypes in his behavioural inhibition model, stating that the difficulty inhibiting behaviour refers only to the Combined and ADHD/HI subtypes. He argues that the primary impairment of the ADHD/I subtype is inattention, rather than problems with inhibition of responses. Thus, there appears to be support for the existence of the two subtypes which suggests that studies that combine these samples are problematic and the conclusions drawn from them may be flawed. Consequently, this study compared working memory performance in children diagnosed with the two distinct ADHD subtypes and also compared these abilities to those of children without ADHD. Despite the inconsistencies in the literature in the area, it is necessary to provide a brief review of the predominant findings against which the results of this study can be evaluated. Two relatively recent meta-analytic reviews provide confirmatory evidence of working memory deficits in children with ADHD relative to controls, even after controlling for co-morbid learning and language disorders, intelligence and reading achievement (Martinussen et al. 2005, Willcutt et al. 2005). Many studies report normal STM verbal storage (most commonly assessed with the Digits Forwards task) in children with ADHD (Lazar and Frank 1998, Williams et al. 2000, Rucklidge and Tannock 2002). However, when assessed on the Digits Backwards task (verbal STM storage plus complex processing), these children perform significantly worse than controls (McInnes et al. 2003). This suggests that passive span is not affected in children with ADHD, as Forward Digit Span makes demands primarily on the phonological loop and articulatory rehearsal processes, while Digits Backwards draws on these processes as well as on the central executive. There are considerably fewer studies that have investigated visuo-spatial working memory in children with ADHD. Visual span tasks are a visual analogue to the Digits Forwards task and require the child to reproduce a sequence of locations on a display demonstrated first by the researcher. Such tests are generally used to assess passive visuo-spatial storage in working memory. Significantly lower performance has been found on such tasks by children with ADHD compared to controls (Kempton et al. 1999, Williams et al. 2000, Barnett et al. 2001, Tripp, Ryan and Pearce 2002, McInnes et al. 2003). However, of the reported studies, many did not control for IQ differences between the ADHD and control groups (e.g. Tripp et al. 2002, McInnes et al. 2003)
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or included samples that had not been formally diagnosed with ADHD (e.g. Williams et al. 2000). In the two studies where ADHD and control groups were matched for IQ and age (e.g. Kempton et al. 1999, Barnett et al. 2001), spatial span deficits were still evident, suggesting deficits in visuo-spatial STM in children with ADHD. Given the impairment in central executive functioning predicted by many theories of ADHD, it is surprising that there is minimal literature on complex span tasks that evaluate these aspects of working memory in this population. Three studies demonstrate no impairment in children with ADHD relative to controls matched for IQ on such tasks (Siegel and Ryan 1989, Kunsti, Oosterlaan and Stevenson 2001, Willcutt, Pennington and Boada 2001). The only exception to this pattern is a study by Cohen et al. (2000), who found that children with ADHD performed below the normative mean on such tasks, but were not significantly different from a control group of children with other psychological disorders. The complex span tasks used in these studies focused on the verbal processing components of working memory. None of the reviewed studies drew comparisons between the different subtypes of ADHD in their samples and only 30% reported subtype ratios. Thus, the review of documented studies shows that there appears to be evidence for a deficit in non-verbal/visuo-spatial STM tasks but not in verbal STM tasks, while complex verbal working memory does not appear to be impaired. However, these findings may be related the age of the sample, since Westerberg et al. (2004) found that a test of visuo-spatial working memory (STM and complex processing combined) discriminated between older children and adolescents (aged 12–15 years) with ADHD and controls, but not between younger children (aged 7.5–11.5 years). This suggests that complex visuo-spatial working memory may not be impaired in young children with ADHD and may be a sensitive measure of cognitive deficits in older children with the disorder. Thus, the issue is complicated by developmental differences in working memory. Developmental studies suggest a fundamental transformation in children’s use of working memory, changing from primarily visual encoding before school entry to a combined visual-verbal strategy within the first years of formal schooling, to finally the adult-like reliance on the verbal subsystem (Palmer 2000, Pickering 2001). Consequently, it would be useful to investigate whether children with ADHD/I and ADHD/HI demonstrate the typical pattern of working memory development. Aims of the study This study was novel in its attempt to compare the performance of children with predominantly inattentive (ADHD/I) and predominantly hyperactive/impulsive (ADHD/HI) ADHD and a control group without any symptoms of ADHD on both verbal and non-verbal working memory tasks. The aim was to address the following questions: 1. Do the ADHD groups have deficits in verbal or spatial working memory? It was anticipated that the children with ADHD would show impaired performance relative to the controls on non-verbal STM, but not on verbal STM, nor on any aspects of complex working memory processing. 2. Do children with the different subtypes of ADHD have differential deficits on verbal versus spatial working memory tasks? It was anticipated that they would be equally impaired in both tasks, suggesting a generalised impairment in working memory. 3. Do children with the different subtypes of ADHD show similar profiles of strength and weakness in the various aspects of working memory (storage versus processing and verbal versus non-verbal) than controls? It was anticipated that they would be better at storage as opposed to processing and at visuo-spatial as opposed to verbal tasks, as is the pattern in typically developing children of this age. Method A between-subjects ex post facto research design was used to investigate whether there were differences in the working memory of children diagnosed with ADHD, predominantly inattentive subtype and ADHD, predominantly hyperactive/impulsive subtype and a control group of children with no symptoms of ADHD.
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Journal of Child and Adolescent Mental Health 2011, 23(2): 107–118
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Participants There were three groups of participants: ADHD/I (n = 27), ADHD/HI (n = 25) and a comparison group (n = 20). They were aged between 6.6–11.25 years. As shown in Table 1, there were no significant group differences in terms of age. The children with ADHD were recruited from four special education schools and were matched exactly for grade, gender and ethnicity, and within six months for age, to a control group of children recruited from three mainstream primary schools. The participants came from middle to upper socio-economic backgrounds and their home language and language of tuition was English. Inclusion criteria for the ADHD groups: These children had all been diagnosed with one of the subtypes of ADHD by their respective school psychologists using the DSM-IV-TR (APA 1994) criteria, the Conners’ Rating Scale-Revised (CRS-R) (Conners et al. 1998a) and the Wechsler Intelligence Scale for Children (Fourth Edition) (WISC-IV), as part of the criteria for entry to the remedial schools. Children were included in the study if their Full Scale IQ on the WISC-IV was in the average range (1Q > 85) and they met the Conner’s and DSM criteria for diagnosis. As shown in Table 1, there were no significant differences between the Full Scale WISC-IV scores of the two ADHD groups. The children were requested not to take their ADHD medication for 24 hours before testing. Only those children whose parents agreed to this could be included. This was an important requirement as psycho-stimulant medication may affect visuo-spatial working memory performance (Sinha, Sagar and Mehta 2008). Participants whose parents agreed to this condition brought their medication with them to school and took it after the tests were complete. Exclusion criteria for the ADHD groups: Children with co-morbid anxiety disorders, sensory, motor or neurological impairment, seizure disorders, psychosis, pervasive developmental disorder or mood disorder were excluded from this study. For this reason fewer than 50% of the sample had co-morbid disorders. As shown in Table 1, the ADHD/HI group had significantly more co-morbid disorders than the ADHD/I group. Inclusion criteria for the comparison group: The children in the control group were all assessed for absence of ADHD symptomatology using the DSM-IV-TR (APA 1994) criteria and the Conners’ Rating Scale- Revised (Conners et al. 1998a). In addition, they were screened for the absence of behavioural problems on the Conners’ Parent and Teacher Rating Scales-Revised (Conners et al. 1998b). Specifically, these children had to exhibit fewer than six symptoms of inattention and fewer than six symptoms of hyperactivity-impulsivity, as rated by parents and teachers on the
Table 1: Descriptive characteristics of matched groups of children with ADHD and control group
Variable Age Gender (male/female) WISC IV
ADHD/I (n = 27) Mean SD 9.1 2.89 18/9 92
ADHD/HI (n = 25) Mean SD 9.3 3.75 15/10
10.09
93
Control (n =20) Mean SD 8.54 2.3 10/10
13.54
Comorbidity rates ODD CD LD
0 4 0
4 1 5
0 0 0
DCD
0
1
0
F 1.32 p = 0.07 0.07a p = 0.10 2.3 p = 0.07 9.97a * p = 0.03
*p F
