Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-23T21:20:11.769Z Has data issue: false hasContentIssue false

Mechanisms underpinning inattention and hyperactivity: neurocognitive support for ADHD dimensionality

Published online by Cambridge University Press:  25 April 2014

G. A. Salum*
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil Federal University of Rio Grande do Sul, Porto Alegre, Brazil
E. Sonuga-Barke
Affiliation:
Southampton University, UK Ghent University, Belgium
J. Sergeant
Affiliation:
Vrije Universiteit, The Netherlands
J. Vandekerckhove
Affiliation:
University of California, USA
A. Gadelha
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil Federal University of Rio Grande do Sul, Porto Alegre, Brazil
T. S. Moriyama
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil São Paulo University, Brazil
A. S. Graeff-Martins
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil São Paulo University, Brazil
G. G. Manfro
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil Federal University of Rio Grande do Sul, Porto Alegre, Brazil
G. Polanczyk
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil São Paulo University, Brazil
L. A. P. Rohde
Affiliation:
National Institute of Developmental Psychiatry for Children and Adolescents, São Paulo, Brazil Federal University of Rio Grande do Sul, Porto Alegre, Brazil
*
*Address for correspondence: G. A. Salum, M.D., Ph.D., Hospital de Clínicas de Porto Alegre, Ramiro Barcelos 2350, room 2202, Porto Alegre 90035-003, Brazil. (Email:gsalumjr@gmail.com)

Abstract

Background.

Taxometric and behavioral genetic studies suggest that attention deficit hyperactivity disorder (ADHD) is best modeled as a dimension rather than a category. We extended these analyses by testing for the existence of putative ADHD-related deficits in basic information processing (BIP) and inhibitory-based executive function (IB-EF) in individuals in the subclinical and full clinical ranges. Consistent with the dimensional model, we predicted that ADHD-related deficits would be expressed across the full spectrum, with the degree of deficit linearly related to the severity of the clinical presentation.

Method.

A total of 1547 children (aged 6–12 years) participated in the study. The Development and Well-Being Assessment (DAWBA) was used to classify children into groups according to levels of inattention and hyperactivity independently: (1) asymptomatic, (2) subthreshold minimal, (3) subthreshold moderate and (4) clinical ADHD. Neurocognitive performance was evaluated using a two-choice reaction time task (2C-RT) and a conflict control task (CCT). BIP and IB-EF measures were derived using a diffusion model (DM) for decomposition of reaction time (RT) and error data.

Results.

Deficient BIP was found in subjects with minimal, moderate and full ADHD defined in terms of inattention (in both tasks) and hyperactivity/impulsivity dimensions (in the 2C-RT). The size of the deficit increased in a linear manner across increasingly severe presentations of ADHD. IB-EF was unrelated to ADHD.

Conclusions.

Deficits in BIP operate at subclinical and clinical levels of ADHD. The linear nature of this relationship provides support for a dimensional model of ADHD in which diagnostic thresholds are defined in terms of clinical and societal burden rather than representing discrete pathophysiological states.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Angold, A, Erkanli, A, Copeland, W, Goodman, R, Fisher, PW, Costello, EJ (2012). Psychiatric diagnostic interviews for children and adolescents: a comparative study. Journal of the American Academy of Child and Adolescent Psychiatry 51, 506517.Google Scholar
Barkley, RA (1997). Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychological Bulletin 121, 6594.Google Scholar
Bitsakou, P, Psychogiou, L, Thompson, M, Sonuga-Barke, EJ (2008). Inhibitory deficits in attention-deficit/hyperactivity disorder are independent of basic processing efficiency and IQ. Journal of Neural Transmission 115, 261268.CrossRefGoogle ScholarPubMed
Carson, RC (1991). Dilemmas in the pathway of the DSM-IV. Journal of Abnormal Psychology 100, 302307.Google Scholar
Castellanos, FX, Sonuga-Barke, EJ, Scheres, A, Di Martino, A, Hyde, C, Walters, JR (2005). Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability. Biological Psychiatry 57, 14161423.CrossRefGoogle ScholarPubMed
Chamberlain, SR, Robbins, TW, Winder-Rhodes, S, Muller, U, Sahakian, BJ, Blackwell, AD, Barnett, JH (2011). Translational approaches to frontostriatal dysfunction in attention-deficit/hyperactivity disorder using a computerized neuropsychological battery. Biological Psychiatry 69, 11921203.Google Scholar
Cho, SC, Kim, BN, Kim, JW, Rohde, LA, Hwang, JW, Chungh, DS, Shin, MS, Lyoo, IK, Go, BJ, Lee, SE, Kim, HW (2009). Full syndrome and subthreshold attention-deficit/hyperactivity disorder in a Korean community sample: comorbidity and temperament findings. European Child and Adolescent Psychiatry 18, 447457.CrossRefGoogle Scholar
Clark, LA, Watson, D, Reynolds, S (1995). Diagnosis and classification of psychopathology: challenges to the current system and future directions. Annual Review of Psychology 46, 121153.Google Scholar
Coghill, D, Sonuga-Barke, EJ (2012). Annual research review: categories versus dimensions in the classification and conceptualisation of child and adolescent mental disorders – implications of recent empirical study. Journal of Child Psychology and Psychiatry, and Allied Disciplines 53, 469489.CrossRefGoogle ScholarPubMed
Coghill, DR, Rhodes, SM, Matthews, K (2007). The neuropsychological effects of chronic methylphenidate on drug-naive boys with attention-deficit/hyperactivity disorder. Biological Psychiatry 62, 954962.Google Scholar
Cohen, J (1988). Statistical Power Analysis for the Behavioral Sciences. Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Faraone, SV, Biederman, J, Doyle, A, Murray, K, Petty, C, Adamson, JJ, Seidman, L (2006). Neuropsychological studies of late onset and subthreshold diagnoses of adult attention-deficit/hyperactivity disorder. Biological Psychiatry 60, 10811087.Google Scholar
Faraone, SV, Kunwar, A, Adamson, J, Biederman, J (2009). Personality traits among ADHD adults: implications of late-onset and subthreshold diagnoses. Psychological Medicine 39, 685693.Google Scholar
Frazier, TW, Youngstrom, EA, Naugle, RI (2007). The latent structure of attention-deficit/hyperactivity disorder in a clinic-referred sample. Neuropsychology 21, 4564.Google Scholar
Goodman, R, Ford, T, Richards, H, Gatward, R, Meltzer, H (2000). The Development and Well-Being Assessment: description and initial validation of an integrated assessment of child and adolescent psychopathology. Journal of Child Psychology and Psychiatry, and Allied Disciplines 41, 645655.CrossRefGoogle ScholarPubMed
Haslam, N (1997). Evidence that male sexual orientation is a matter of degree. Journal of Personality and Social Psychology 73, 862870.Google Scholar
Haslam, N, Williams, B, Prior, M, Haslam, R, Graetz, B, Sawyer, M (2006). The latent structure of attention-deficit/hyperactivity disorder: a taxometric analysis. Australian and New Zealand Journal of Psychiatry 40, 639647.CrossRefGoogle ScholarPubMed
Hogan, AM, Vargha-Khadem, F, Kirkham, FJ, Baldeweg, T (2005). Maturation of action monitoring from adolescence to adulthood: an ERP study. Developmental Science 8, 525534.Google Scholar
Huang-Pollock, CL, Karalunas, SL, Tam, H, Moore, AN (2012). Evaluating vigilance deficits in ADHD: a meta-analysis of CPT performance. Journal of Abnormal Psychology 121, 360371.Google Scholar
Hudziak, JJ, Heath, AC, Madden, PF, Reich, W, Bucholz, KK, Slutske, W, Bierut, LJ, Neuman, RJ, Todd, RD (1998). Latent class and factor analysis of DSM-IV ADHD: a twin study of female adolescents. Journal of the American Academy of Child and Adolescent Psychiatry 37, 848857.CrossRefGoogle ScholarPubMed
Karalunas, SL, Huang-Pollock, CL (2013). Integrating impairments in reaction time and executive function using a diffusion model framework. Journal of Abnormal Child Psychology 41, 837850.Google Scholar
Karalunas, SL, Huang-Pollock, CL, Nigg, JT (2012). Decomposing attention-deficit/hyperactivity disorder (ADHD)-related effects in response speed and variability. Neuropsychology 26, 684694.Google Scholar
Killeen, PR, Russell, VA, Sergeant, JA (2013). A behavioral neuroenergetics theory of ADHD. Neuroscience and Biobehavioral Reviews 37, 625657.Google Scholar
Konrad, K, Gauggel, S, Manz, A, Scholl, M (2000). Lack of inhibition: a motivational deficit in children with attention deficit/hyperactivity disorder and children with traumatic brain injury. Child Neuropsychology 6, 286296.Google Scholar
Krol, NP, De Bruyn, EE, Coolen, JC, van Aarle, EJ (2006). From CBCL to DSM: a comparison of two methods to screen for DSM-IV diagnoses using CBCL data. Journal of Clinical Child and Adolescent Psychology 35, 127135.Google Scholar
Kuntsi, J, Klein, C (2012). Intraindividual variability in ADHD and its implications for research of causal links. Current Topics in Behavioral Neurosciences 9, 6791.CrossRefGoogle ScholarPubMed
Kuntsi, J, Wood, AC, van der Meere, J, Asherson, P (2009). Why cognitive performance in ADHD may not reveal true potential: findings from a large population-based sample. Journal of the International Neuropsychological Society 15, 570579.Google Scholar
Larsson, H, Anckarsater, H, Rastam, M, Chang, Z, Lichtenstein, P (2012). Childhood attention-deficit hyperactivity disorder as an extreme of a continuous trait: a quantitative genetic study of 8,500 twin pairs. Journal of Child Psychology and Psychiatry, and Allied Disciplines 53, 7380.CrossRefGoogle Scholar
Lehmann, EL (1975). Nonparametrics: Statistical Methods Based on Ranks. Holden-Day: San Francisco, CA.Google Scholar
Levy, F, Hay, DA, McStephen, M, Wood, C, Waldman, I (1997). Attention-deficit hyperactivity disorder: a category or a continuum? Genetic analysis of a large-scale twin study. Journal of the American Academy of Child and Adolescent Psychiatry 36, 737744.Google Scholar
Lubke, GH, Hudziak, JJ, Derks, EM, van Bijsterveldt, TC, Boomsma, DI (2009). Maternal ratings of attention problems in ADHD: evidence for the existence of a continuum. Journal of the American Academy of Child and Adolescent Psychiatry 48, 10851093.Google Scholar
Marcus, DK, Barry, TD (2011). Does attention-deficit/hyperactivity disorder have a dimensional latent structure? A taxometric analysis. Journal of Abnormal Psychology 120, 427442.CrossRefGoogle ScholarPubMed
Marcus, DK, Norris, AL, Coccaro, EF (2012). The latent structure of attention deficit/hyperactivity disorder in an adult sample. Journal of Psychiatric Research 46, 782789.CrossRefGoogle Scholar
Matte, B, Rohde, LA, Grevet, EH (2012). ADHD in adults: a concept in evolution. Attention Deficit and Hyperactivity Disorders 4, 5362.Google Scholar
Mulder, MJ, Bos, D, Weusten, JM, van Belle, J, van Dijk, SC, Simen, P, van Engeland, H, Durston, S (2010). Basic impairments in regulating the speed-accuracy tradeoff predict symptoms of attention-deficit/hyperactivity disorder. Biological Psychiatry 68, 11141119.Google Scholar
Neuman, RJ, Todd, RD, Heath, AC, Reich, W, Hudziak, JJ, Bucholz, KK, Madden, PA, Begleiter, H, Porjesz, B, Kuperman, S, Hesselbrock, V, Reich, T (1999). Evaluation of ADHD typology in three contrasting samples: a latent class approach. Journal of the American Academy of Child and Adolescent Psychiatry 38, 2533.CrossRefGoogle ScholarPubMed
Nigg, JT, Willcutt, EG, Doyle, AE, Sonuga-Barke, EJ (2005). Causal heterogeneity in attention-deficit/hyperactivity disorder: do we need neuropsychologically impaired subtypes? Biological Psychiatry 57, 12241230.Google Scholar
Oosterlaan, J, Logan, GD, Sergeant, JA (1998). Response inhibition in AD/HD, CD, comorbid AD/HD + CD, anxious, and control children: a meta-analysis of studies with the stop task. Journal of Child Psychology and Psychiatry, and Allied Disciplines 39, 411425.Google Scholar
Oosterlaan, J, Scheres, A, Sergeant, JA (2005). Which executive functioning deficits are associated with AD/HD, ODD/CD and comorbid AD/HD+ODD/CD? Journal of Abnormal Child Psychology 33, 6985.Google Scholar
Parisi, D (1997). Artificial life and higher level cognition. Brain and Cognition 34, 160184.Google Scholar
Polderman, TJ, Derks, EM, Hudziak, JJ, Verhulst, FC, Posthuma, D, Boomsma, DI (2007). Across the continuum of attention skills: a twin study of the SWAN ADHD rating scale. Journal of Child Psychology and Psychiatry, and Allied Disciplines 48, 10801087.Google Scholar
Quay, HC (1997). Inhibition and attention deficit hyperactivity disorder. Journal of Abnormal Child Psychology 25, 713.Google Scholar
Ranby, KW, Boynton, MH, Kollins, SH, McClernon, FJ, Yang, C, Fuemmeler, BF (2012). Understanding the phenotypic structure of adult retrospective ADHD symptoms during childhood in the United States. Journal of Clinical Child and Adolescent Psychology 41, 261274.Google Scholar
Rapoport, JL, Buchsbaum, MS, Weingartner, H, Zahn, TP, Ludlow, C, Mikkelsen, EJ (1980). Dextroamphetamine. Its cognitive and behavioral effects in normal and hyperactive boys and normal men. Archives of General Psychiatry 37, 933943.Google Scholar
Ratcliff, R, McKoon, G (1988). A retrieval theory of priming in memory. Psychological Review 95, 385408.Google Scholar
Rhodes, SM, Coghill, DR, Matthews, K (2006). Acute neuropsychological effects of methylphenidate in stimulant drug-naive boys with ADHD II – broader executive and non-executive domains. Journal of Child Psychology and Psychiatry, and Allied Disciplines 47, 11841194.Google Scholar
Rhodes, SM, Park, J, Seth, S, Coghill, DR (2012). A comprehensive investigation of memory impairment in attention deficit hyperactivity disorder and oppositional defiant disorder. Journal of Child Psychology and Psychiatry, and Allied Disciplines 53, 128137.Google Scholar
Rommelse, NN, Altink, ME, de Sonneville, LM, Buschgens, CJ, Buitelaar, J, Oosterlaan, J, Sergeant, JA (2007). Are motor inhibition and cognitive flexibility dead ends in ADHD? Journal of Abnormal Child Psychology 35, 957967.Google Scholar
Salum, GA, Mogg, K, Bradley, BP, Gadelha, A, Pan, P, Tamanaha, AC, Moriyama, T, Graeff-Martins, AS, Jarros, RB, Polanczyk, G, do Rosario, MC, Leibenluft, E, Rohde, LA, Manfro, GG, Pine, DS (2013). Threat bias in attention orienting: evidence of specificity in a large community-based study. Psychological Medicine 43, 733745.Google Scholar
Salum, GA, Sergeant, J, Sonuga-Barke, E, Vandekerckhove, J, Gadelha, A, Pan, PM, Moriyama, TS, Graeff-Martins, AS, de Alvarenga, PG, do Rosario, MC, Manfro, GG, Polanczyk, G, Rohde, LA (2014). Specificity of basic information processing and inhibitory control in attention deficit hyperactivity disorder. Psychological Medicine 44, 617631.Google Scholar
Scahill, L, Schwab-Stone, M, Merikangas, KR, Leckman, JF, Zhang, H, Kasl, S (1999). Psychosocial and clinical correlates of ADHD in a community sample of school-age children. Journal of the American Academy of Child and Adolescent Psychiatry 38, 976984.CrossRefGoogle Scholar
Sergeant, J (2000). The cognitive-energetic model: an empirical approach to attention-deficit hyperactivity disorder. Neuroscience and Biobehavioral Reviews 24, 712.CrossRefGoogle Scholar
Sergeant, JA, Geurts, H, Huijbregts, S, Scheres, A, Oosterlaan, J (2003). The top and the bottom of ADHD: a neuropsychological perspective. Neuroscience and Biobehavioral Reviews 27, 583592.Google Scholar
Shaw, P, Gilliam, M, Liverpool, M, Weddle, C, Malek, M, Sharp, W, Greenstein, D, Evans, A, Rapoport, J, Giedd, J (2011). Cortical development in typically developing children with symptoms of hyperactivity and impulsivity: support for a dimensional view of attention deficit hyperactivity disorder. American Journal of Psychiatry 168, 143151.Google Scholar
Slusarek, M, Velling, S, Bunk, D, Eggers, C (2001). Motivational effects on inhibitory control in children with ADHD. Journal of the American Academy of Child and Adolescent Psychiatry 40, 355363.Google Scholar
Sonuga-Barke, EJ (2005). Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biological Psychiatry 57, 12311238.Google Scholar
Surman, C, Hammerness, P, Petty, C, Doyle, R, Chu, N, Gebhard, N, Williams, C, Biederman, J (2010). Atomoxetine in the treatment of adults with subthreshold and/or late onset attention-deficit hyperactivity disorder-not otherwise specified (ADHD-NOS): a prospective open-label 6-week study. CNS Neuroscience and Therapeutics 16, 612.Google Scholar
Swanson, J, Baler, RD, Volkow, ND (2011). Understanding the effects of stimulant medications on cognition in individuals with attention-deficit hyperactivity disorder: a decade of progress. Neuropsychopharmacology 36, 207226.Google Scholar
Vandekerckhove, J, Tuerlinckx, F (2007). Fitting the Ratcliff diffusion model to experimental data. Psychonomic Bulletin and Review 14, 10111026.Google Scholar
Vandekerckhove, J, Tuerlinckx, F, Lee, MD (2011). Hierarchical diffusion models for two-choice response times. Psychological Methods 16, 4462.Google Scholar
Wang, GJ, Volkow, ND, Wigal, T, Kollins, SH, Newcorn, JH, Telang, F, Logan, J, Jayne, M, Wong, CT, Han, H, Fowler, JS, Zhu, W, Swanson, JM (2013). Long-term stimulant treatment affects brain dopamine transporter level in patients with attention deficit hyperactive disorder. PloS One 8, e63023.Google Scholar
Weissman, MM, Wickramaratne, P, Adams, P, Wolk, S, Verdeli, H, Olfson, M (2000). Brief screening for family psychiatric history: the family history screen. Archives of General Psychiatry 57, 675682.CrossRefGoogle ScholarPubMed
White, CN, Ratcliff, R, Vasey, MW, McKoon, G (2010). Using diffusion models to understand clinical disorders. Journal of Mathematical Psychology 54, 3952.Google Scholar
Wood, AC, Buitelaar, J, Rijsdijk, F, Asherson, P, Kuntsi, J (2010). Rethinking shared environment as a source of variance underlying attention-deficit/hyperactivity disorder symptoms: comment on Burt (2009). Psychological Bulletin 136, 331340.Google Scholar
Supplementary material: File

Salum Supplementary Material

Supplementary Material

Download Salum Supplementary Material(File)
File 160.8 KB