Reaction time variability and attention-deficit/hyperactivity disorder: is increased reaction time variability specific to attention-deficit/hyperactivity disorder? Testing predictions from the default-mode interference hypothesis

Giovanni A. Salum1,2, João R. Sato1,3, Arthur G. Manfro4,2, Pedro M. Pan1,5, Ary Gadelha1,5, Maria C. do Rosário1,5, Guilherme V. Polanczyk1, Francisco X. Castellanos6,7, Edmund Sonuga-Barke8,9, Luis A. Rohde1,2,10
1National Institute of Developmental Psychiatry for Children and Adolescents - CNPq, São Paulo, Brazil
2ADHD Outpatient Program, Hospital de Clínicas de Porto Alegre, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
3Universidade Federal do ABC, São Paulo, Brazil
4National Institute of Developmental Psychiatry for Children and Adolescents (CNPq), São Paulo, Brazil
5Universidade Federal de São Paulo, São Paulo, Brazil
6New York University Langone Medical Center, New York, USA
7Nathan Kline Institute, Orangeburg, USA
8Southampton University, Southampton, UK
9Ghent University, Ghent, Belgium
10Universidade de São Paulo, São Paulo, Brazil

Tóm tắt

Increased reaction time variability (RTV) is one of the most replicable behavioral correlates of attention-deficit/hyperactivity disorder (ADHD). However, this may not be specific to ADHD but a more general marker of psychopathology. Here we compare RT variability in individuals with ADHD and those with other childhood internalizing and externalizing conditions both in terms of standard (i.e., the standard deviation of reaction time) and alternative indices that capture low-frequency oscillatory patterns in RT variations over time thought to mark periodic lapses of attention in ADHD. A total of 667 participants (6–12 years old) were classified into non-overlapping diagnostic groups consisting of children with fear disorders (n = 91), distress disorders (n = 56), ADHD (n = 103), oppositional defiant or conduct disorder (ODD/CD; n = 40) and typically developing controls (TDC; n = 377). We used a simple two-choice reaction time task to measure reaction time. The strength of oscillations in RTs across the session was extracted using spectral analyses. Higher RTV was present in ADHD compared to all other disorder groups, effects that were equally strong across all frequency bands. Interestingly, we found that lower RTV to characterize ODD/CD relative to TDC, a finding that was more pronounced at lower frequencies. In general, our data support RTV as a specific marker of ADHD. RT variation across time in ADHD did not show periodicity in a specific frequency band, not supporting that ADHD RTV is the product of spontaneous periodic lapses of attention. Low-frequency oscillations may be particularly useful to differentiate ODD/CD from TDC.

Tài liệu tham khảo

Adamo N, Di Martino A, Esu L, Petkova E, Johnson K, Kelly S, Zuddas A (2012) Increased response-time variability across different cognitive tasks in children with ADHD. J Atten Disord. https://doi.org/10.1177/1087054712439419 Adamo N, Huo L, Adelsberg S, Petkova E, Castellanos FX, Di Martino A (2014) Response time intra-subject variability: commonalities between children with autism spectrum disorders and children with ADHD. Eur Child Adolesc Psychiatr 23(2):69–79. https://doi.org/10.1007/s00787-013-0428-4 Angold A, Erkanli A, Copeland W, Goodman R, Fisher PW, Costello EJ (2012) Psychiatric diagnostic interviews for children and adolescents: a comparative study. J Am Acad Child Adolesc Psychiatry 51(5):506–517. https://doi.org/10.1016/j.jaac.2012.02.020 Biederman J, Kwon A, Aleardi M, Chouinard VA, Marino T, Cole H, Faraone SV (2005) Absence of gender effects on attention deficit hyperactivity disorder: findings in nonreferred subjects. Am J Psychiatry 162(6):1083–1089. https://doi.org/10.1176/appi.ajp.162.6.1083 Bron TI, Bijlenga D, Boonstra AM, Breuk M, Pardoen WFH, Beekman ATF, Kooij JJS (2014) OROS-methylphenidate efficacy on specific executive functioning deficits in adults with ADHD: a randomized, placebo-controlled cross-over study. Eur Neuropsychopharmacol 24(4):519–528. https://doi.org/10.1016/j.euroneuro.2014.01.007 Broyd SJ, Demanuele C, Debener S, Helps SK, James CJ, Sonuga-Barke EJ (2009) Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci Biobehav Rev 33(3):279–296. https://doi.org/10.1016/j.neubiorev.2008.09.002 Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304(5679):1926–1929. https://doi.org/10.1126/science.1099745 Castellanos FX, Tannock R (2002) Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nat Rev Neurosci 3(8):617–628. https://doi.org/10.1038/nrn896 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. Biol Psychiatry 57(11):1416–1423. https://doi.org/10.1016/j.biopsych.2004.12.005 Di Martino A, Ghaffari M, Curchack J, Reiss P, Hyde C, Vannucci M, Castellanos FX (2008) Decomposing intra-subject variability in children with attention-deficit/hyperactivity disorder. Biol Psychiatry 64(7):607–614. https://doi.org/10.1016/j.biopsych.2008.03.008 Figueiredo VLM (2001) Uma adaptação brasileira do teste de inteligência WISC-III. Curso de Pós-Graduação em Psicologia, Instituto de Psicologia—Universidade de Brasília. Brasília, DF Foreman D, Morton S, Ford T (2009) Exploring the clinical utility of the development and well-being assessment (DAWBA) in the detection of hyperkinetic disorders and associated diagnoses in clinical practice. J Child Psychol Psychiatry 50(4):460–470. https://doi.org/10.1111/j.1469-7610.2008.02017.x Fransson P, Skiold B, Horsch S, Nordell A, Blennow M, Lagercrantz H, Aden U (2007) Resting-state networks in the infant brain. Proc Natl Acad Sci USA 104(39):15531–15536. https://doi.org/10.1073/pnas.0704380104 Gescheider GA, Guclu B, Sexton JL, Karalunas S, Fontana A (2005) Spatial summation in the tactile sensory system: probability summation and neural integration. Somatosens Mot Res 22(4):255–268. https://doi.org/10.1080/08990220500420236 Geurts HM, Grasman RP, Verte S, Oosterlaan J, Roeyers H, van Kammen SM, Sergeant JA (2008) Intra-individual variability in ADHD, autism spectrum disorders and Tourette’s syndrome. Neuropsychologia 46(13):3030–3041. https://doi.org/10.1016/j.neuropsychologia.2008.06.013 Gilden DL (2009) Global model analysis of cognitive variability. Cogn Sci 33(8):1441–1467. https://doi.org/10.1111/j.1551-6709.2009.01060.x Gilden DL, Thornton T, Mallon MW (1995) 1/f noise in human cognition. Science 267(5205):1837–1839 Gillberg C, Gillberg IC, Rasmussen P, Kadesjo B, Soderstrom H, Rastam M, Niklasson L (2004) Co-existing disorders in ADHD—implications for diagnosis and intervention. Eur Child Adolesc Psychiatry 13(Suppl 1):I80–I92. https://doi.org/10.1007/s00787-004-1008-4 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. J Child Psychol Psychiatry 41(5):645–655 Goodman A, Heiervang E, Collishaw S, Goodman R (2011) The ‘DAWBA bands’ as an ordered-categorical measure of child mental health: description and validation in British and Norwegian samples. Soc Psychiatry Psychiatr Epidemiol 46(6):521–532. https://doi.org/10.1007/s00127-010-0219-x Helps SK, Broyd SJ, Bitsakou P, Sonuga-Barke EJ (2011) Identifying a distinctive familial frequency band in reaction time fluctuations in ADHD. Neuropsychology 25(6):711–719. https://doi.org/10.1037/a0024479 Hervey AS, Epstein JN, Curry JF, Tonev S, Eugene Arnold L, Keith Conners C, Hechtman L (2006) Reaction time distribution analysis of neuropsychological performance in an ADHD sample. Child Neuropsychol 12(2):125–140. https://doi.org/10.1080/09297040500499081 Hogan AM, Vargha-Khadem F, Kirkham FJ, Baldeweg T (2005) Maturation of action monitoring from adolescence to adulthood: an ERP study. Dev Sci 8(6):525–534. https://doi.org/10.1111/j.1467-7687.2005.00444.x Huang-Pollock CL, Karalunas SL, Tam H, Moore AN (2012) Evaluating vigilance deficits in ADHD: a meta-analysis of CPT performance. J Abnorm Psychol 121(2):360–371. https://doi.org/10.1037/a0027205 Johnson KA, Kelly SP, Bellgrove MA, Barry E, Cox M, Gill M, Robertson IH (2007) Response variability in attention deficit hyperactivity disorder: evidence for neuropsychological heterogeneity. Neuropsychologia 45(4):630–638. https://doi.org/10.1016/j.neuropsychologia.2006.03.034 Johnson KA, Barry E, Bellgrove MA, Cox M, Kelly SP, Daibhis A, Gill M (2008) Dissociation in response to methylphenidate on response variability in a group of medication naive children with ADHD. Neuropsychologia 46(5):1532–1541. https://doi.org/10.1016/j.neuropsychologia.2008.01.002 Kapur S, Phillips AG, Insel TR (2012) Why has it taken so long for biological psychiatry to develop clinical tests and what to do about it? Mol Psychiatry. https://doi.org/10.1038/mp.2012.105 Karalunas SL, Huang-Pollock CL, Nigg JT (2012a) Decomposing attention-deficit/hyperactivity disorder (ADHD)-related effects in response speed and variability. Neuropsychology 26(6):684–694. https://doi.org/10.1037/a0029936 Karalunas SL, Huang-Pollock CL, Nigg JT (2012b) Is reaction time variability in ADHD mainly at low frequencies? J Child Psychol Psychiatry. https://doi.org/10.1111/jcpp.12028 Karalunas SL, Geurts HM, Konrad K, Bender S, Nigg JT (2014) Annual research review: reaction time variability in ADHD and autism spectrum disorders: measurement and mechanisms of a proposed trans-diagnostic phenotype. J Child Psychol Psychiatry 55(6):685–710. https://doi.org/10.1111/jcpp.12217 Karantinos T, Tsoukas E, Mantas A, Kattoulas E, Stefanis NC, Evdokimidis I, Smyrnis N (2014) Increased intra-subject reaction time variability in the volitional control of movement in schizophrenia. Psychiatry Res 215(1):26–32. https://doi.org/10.1016/j.psychres.2013.10.031 Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE (2005) Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the national comorbidity survey replication. Arch Gen Psychiatry 62(6):617–627. https://doi.org/10.1001/archpsyc.62.6.617 Klein C, Wendling K, Huettner P, Ruder H, Peper M (2006) Intra-subject variability in attention-deficit hyperactivity disorder. Biol Psychiatry 60(10):1088–1097. https://doi.org/10.1016/j.biopsych.2006.04.003 Kofler MJ, Rapport MD, Sarver DE, Raiker JS, Orban SA, Friedman LM, Kolomeyer EG (2013) Reaction time variability in ADHD: a meta-analytic review of 319 studies. Clin Psychol Rev 33(6):795–811. https://doi.org/10.1016/j.cpr.2013.06.001 Kofler MJ, Alderson RM, Raiker JS, Bolden J, Sarver DE, Rapport MD (2014) Working memory and intraindividual variability as neurocognitive indicators in ADHD: examining competing model predictions. Neuropsychology 28(3):459–471. https://doi.org/10.1037/neu0000050 Kuhn S, Schmiedek F, Schott B, Ratcliff R, Heinze HJ, Duzel E, Lovden M (2011) Brain areas consistently linked to individual differences in perceptual decision-making in younger as well as older adults before and after training. J Cogn Neurosci 23(9):2147–2158. https://doi.org/10.1162/jocn.2010.21564 Kuntsi J, Klein C (2012) Intraindividual variability in ADHD and its implications for research of causal links. Curr Top Behav Neurosci 9:67–91. https://doi.org/10.1007/7854_2011_145 Leth-Steensen C, Elbaz ZK, Douglas VI (2000) Mean response times, variability, and skew in the responding of ADHD children: a response time distributional approach. Acta Psychol (Amst) 104(2):167–190 Maniadaki K, Sonuga-Barke E, Kakouros E (2006) Adults’ self-efficacy beliefs and referral attitudes for boys and girls with AD/HD. Eur Child Adolesc Psychiatry 15(3):132–140. https://doi.org/10.1007/s00787-005-0514-3 Martel MM, Pan PM, Hoffmann MS, Gadelha A, do Rosário MC, Mari JJ, Manfro GG, Miguel EC, Paus T, Bressan RA, Rohde LA, Salum GA, (2017) A general psychopathology factor (P factor) in children: Structural model analysis and external validation through familial risk and child global executive function. J Abnorm Psychol 126(1):137–148. https://doi.org/10.1037/abn0000205 Metin B, Roeyers H, Wiersema JR, van der Meere JJ, Thompson M, Sonuga-Barke E (2013) ADHD performance reflects inefficient but not impulsive information processing: a diffusion model analysis. Neuropsychology 27(2):193–200. https://doi.org/10.1037/a0031533 Nagel BJ, Bathula D, Herting M, Schmitt C, Kroenke CD, Fair D, Nigg JT (2011) Altered white matter microstructure in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 50(3):283–292. https://doi.org/10.1016/j.jaac.2010.12.003 Penttonen M, Buzsáki G (2003) Natural logarithmic relationship between brain oscillators. Thal Relat Syst 2:145–152 Philiastides MG, Auksztulewicz R, Heekeren HR, Blankenburg F (2011) Causal role of dorsolateral prefrontal cortex in human perceptual decision making. Curr Biol 21(11):980–983. https://doi.org/10.1016/j.cub.2011.04.034 Sagvolden T, Johansen EB, Aase H, Russell VA (2005) A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav Brain Sci 28(3):397–419. https://doi.org/10.1017/s0140525x05000075 (discussion 419–368) Salum GA, Sergeant J, Sonuga-Barke E, Vandekerckhove J, Gadelha A, Pan PM, Rohde LA (2014a) Specificity of basic information processing and inhibitory control in attention deficit hyperactivity disorder. Psychol Med 44(3):617–631. https://doi.org/10.1017/S0033291713000639 Salum GA, Sonuga-Barke E, Sergeant J, Vandekerckhove J, Gadelha A, Moriyama TS, Rohde LA (2014b) Mechanisms underpinning inattention and hyperactivity: neurocognitive support for ADHD dimensionality. Psychol Med 44(15):3189–3201. https://doi.org/10.1017/S0033291714000919 Salum GA, Gadelha A, Pan PM, Moriyama TS, Graeff-Martins AS, Tamanaha AC, Rohde LA (2015) High risk cohort study for psychiatric disorders in childhood: rationale, design, methods and preliminary results. Int J Methods Psychiatr Res 24(1):58–73. https://doi.org/10.1002/mpr.1459 Sonuga-Barke EJ (2011) Editorial: ADHD as a reinforcement disorder—moving from general effects to identifying (six) specific models to test. J Child Psychol Psychiatry 52(9):917–918. https://doi.org/10.1111/j.1469-7610.2011.02444.x Sonuga-Barke EJ, Castellanos FX (2007) Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neurosci Biobehav Rev 31(7):977–986. https://doi.org/10.1016/j.neubiorev.2007.02.005 Tellegen A, Briggs PF (1967) Old wine in new skins: grouping Wechsler subtests into new scales. J Consult Psychol 31(5):499–506 Tye Charlotte, Johnson Katherine A, Kelly Simon P, Asherson Philip, Kuntsi Jonna, Ashwood Karen L, Azadi Bahare, Bolton Patrick, McLoughlin Gráinne (2016) Response time variability under slow and fast-incentive conditions in children with ASD, ADHD and ASD + ADHD. J Child Psychol Psychiatry 57(12):1414–1423. https://doi.org/10.1111/jcpp.12608 van Belle J, van Hulst BM, Durston S (2015a) Developmental differences in intra-individual variability in children with ADHD and ASD. J Child Psychol Psychiatry. https://doi.org/10.1111/jcpp.12417 van Belle J, van Raalten T, Bos DJ, Zandbelt BB, Oranje B, Durston S (2015b) Capturing the dynamics of response variability in the brain in ADHD. Neuroimage Clin 7:132–141. https://doi.org/10.1016/j.nicl.2014.11.014 Wechsler D (2002) WISC-III: Escala de Inteligência Wechsler para Crianças: Manual, vol 3a. Casa do Psicólogo, São Paulo Weissman MM, Wickramaratne P, Adams P, Wolk S, Verdeli H, Olfson M (2000) Brief screening for family psychiatric history: the family history screen. Arch Gen Psychiatry 57(7):675–682 Williams BR, Strauss EH, Hultsch DF, Hunter MA, Tannock R (2007) Reaction time performance in adolescents with attention deficit/hyperactivity disorder: evidence of inconsistency in the fast and slow portions of the RT distribution. J Clin Exp Neuropsychol 29(3):277–289. https://doi.org/10.1080/13803390600678020