What Part of Working Memory is not Working in ADHD? Short-Term Memory, the Central Executive and Effects of Reinforcement
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Abstract
Deficits in Working Memory (WM) are related to symptoms of Attention-Deficit/Hyperactivity Disorder (ADHD). In children with ADHD visuospatial WM is most impaired. WM is composed of Short-Term Memory (STM) and a Central Executive (CE). Therefore, deficits in either or both STM and the CE may account for WM impairments in children with ADHD. WM-component studies investigating this find deficits in both STM and the CE. However, recent studies show that not only cognitive deficits, but also motivational deficits give rise to the aberrant WM performance of children with ADHD. To date, the influence of these motivational deficits on the components of WM has not been investigated. This study examined the effects of a standard (feedback-only) and a high level of reinforcement (feedback + 10 euros) on the visuospatial WM-, visuospatial STM-, and the CE performance of 86 children with ADHD and 62 typically-developing controls. With standard reinforcement the STM, CE, and WM performance of children with ADHD was worse than that of controls. High reinforcement improved STM and WM performance more in children with ADHD than in controls, but was unable to normalize their performance. High reinforcement did not appear to improve the CE-related performance of children with ADHD and controls. Motivational deficits have a detrimental effect on both the visuospatial WM performance and the STM performance of children with ADHD. Aside from motivational deficits, both the visuospatial STM and the CE of children with ADHD are impaired, and give rise to their deficits in visuospatial WM.
Keywords
ADHD Working-memory Motivation Short-term-memory Central-executive ReinforcementNotes
Acknowledgments
We are grateful to Jeugdriagg Noord Holland Zuid, GGz Noord Holland Noord (Centrum voor Kinder- en Jeugdpsychiatrie), Regionaal Centrum voor Kinder en Jeugdpsychiatrie Gooi en Vechtstreek (RCKJP), Bosman GGz, Stichting De Praktijk, Stichting Kram, PuntP, Academisch Behandelcentrum UvA Minds, Kinderpraktijk VIS and the participating schools (OBS De Weidevogel, Amsterdam; OBS De Witte Olifant, Amsterdam; De Dr. E. Boekmanschool, Amsterdam; OBS Jules Verne, Alkmaar; PCBS Van der Brugghenschool, Huizen; Montessorischool De Boog, Nieuw-Vennep; and De Willemsparkschool, Amsterdam), to Thomas Gladwin for his comments and statistical advice, to Jasper Wijnen for programming the task, to Tim van den Broek, Josje de Bont, Annette Brouwer, Tycho Dekkers, Lucie van den Eertwegh, Roza van der Heide, Lisanne Klink, Astrid Nauta, Inge Meulenberg, Muriël Musa, Pascale Riaskoff, Elise Tilma, Marije Voermans, Ida de Vries, and Pamina Warmbrunn for their help with data collection, and to all participating children and families.
Disclosures
SvdO has been a paid consultant for Janssen pharmaceuticals in the development and evaluation of a serious game “Heelseeker” aimed at training cognitive functions.
References
- Aarts, E., van Holstein, M., & Cools, R. (2011). Striatal dopamine and the interface between motivation and cognition. Frontiers in Psychology, 2, 163.PubMedCrossRefGoogle Scholar
- Alderson, R. M., Rapport, M. D., Hudec, K. L., Sarver, D. E., & Kofler, M. J. (2010). Competing core processes in attention-deficit/hyperactivity disorder (ADHD): do working memory deficiencies underlie behavioral inhibition deficits? Journal of Abnormal Child Psychology, 38, 497–507.PubMedCrossRefGoogle Scholar
- American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders, 4th revised edition (DSM-IV-TR). Washington, DC: American Psychiatric Association.CrossRefGoogle Scholar
- Baddeley, A. (2003). Working memory: looking back and looking forward. Nature Neuroscience, 4, 829–839.Google Scholar
- Baddeley, A. D. (2007). Working memory, thought and action. Oxford: Oxford University Press.CrossRefGoogle Scholar
- Baddeley, A. (2010). Working memory. Current Biology, 20, R136–R140.PubMedCrossRefGoogle Scholar
- Baddeley, A. D., & Hitch, G. (1974). Working memory. In G. A. Bower (Ed.), The psychology of learning and motivation (Vol. 8, pp. 47–89). New York: Academic.Google Scholar
- Barkley, R. A. (2006). Attention-deficit hyperactivity disorder. A handbook for diagnosis and treatment (3rd ed.). New York: Guilford Press.Google Scholar
- Beck, S. J., Hanson, C. A., Puffenberger, S. S., Benninger, K. L., & Benninger, W. B. (2010). A controlled trial of working memory training for children and adolescents with ADHD. Journal of Clinical Child and Adolescent Psychology, 39, 825–836.PubMedCrossRefGoogle Scholar
- Burgess, G. C., Depue, B. E., Ruzic, L., Willcutt, E. G., Du, Y. P., & Banich, M. T. (2010). Attentional control activation relates to working memory in attention-deficit/hyperactivity disorder. Biological Psychiatry, 67, 632–640.PubMedCrossRefGoogle Scholar
- Castellanos, F. X., Sonuga-Barke, E. J. S., Milham, M. P., & Tannock, R. (2006). Characterizing cognition in ADHD: beyond executive dysfunction. Trends in Cognitive Sciences, 10, 117–123.PubMedCrossRefGoogle Scholar
- Conway, A. R. A., Jarrold, C., Kane, M. J., Miyake, A., & Towse, J. (2007). Variation in working memory: An introduction. In A. R. A. Conway, C. Jarrold, M. J. Kane, A. Miyake, & J. Towse (Eds.), Variation in working memory. Oxford: Oxford University Press.Google Scholar
- Cools, R., & D’Esposito, M. (2011). Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biological Psychiatry, 69, 113–125.CrossRefGoogle Scholar
- Corsi, P. M. (1972). Human memory and the medial temporal region of the brain. Dissertation Abstracts International, 34, 819B.Google Scholar
- Cowan, N. (1995). Attention and memory: An integrated framework. Oxford, England: Oxford University Press.Google Scholar
- Delaney, H. D., & Maxwell, S. E. (1981). On using analysis of covariance in repeated measures designs. Multivariate Behavioral Research, 16, 105–123.CrossRefGoogle Scholar
- Demurie, E., Roeyers, H., Baeyens, D., & Sonuga-Barke, E. J. S. (2011). Common alterations in sensitivity to type but not amount of reward in ADHD and autism spectrum disorders. Journal of Child Psychology and Psychiatry, 52, 1164–1173.PubMedCrossRefGoogle Scholar
- Dennis, M., Francis, D. J., Cirino, P. T., Schachar, R., Barnes, M. A., & Fletcher, J. M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society: JINS, 15, 331–343.PubMedCrossRefGoogle Scholar
- Diamond, A. (2005). Attention-deficit disorder (attention-deficit/hyperactivity disorder without hyperactivity): a neurobiologically and behaviorally distinct disorder from attention-deficit/hyperactivity disorder (with hyperactivity). Development and Psychopathology, 17, 807–825.PubMedCrossRefGoogle Scholar
- Dovis, S., Van der Oord, S., Wiers, R. W., & Prins, P. J. M. (2012). Can motivation normalize working memory and task persistence in children with attention-deficit/hyperactivity disorder? The effects of money and computer-gaming. Journal of Abnormal Child Psychology, 40, 669–681.PubMedCrossRefGoogle Scholar
- Durstewitz, D., & Seamans, J. K. (2002). The computational role of dopamine D1 receptors in working memory. Neural Networks, 15, 561–572.PubMedCrossRefGoogle Scholar
- Durstewitz, D., & Seamans, J. K. (2008). The dual-state theory of prefrontal cortex dopamine function with relevance to catechol-o-methyltransferase genotypes and schizophrenia. Biological Psychiatry, 64, 739–749.PubMedCrossRefGoogle Scholar
- Engle, R. W., Tuholski, S. W., Laughlin, J. E., & Conway, A. R. A. (1999). Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. Journal of Experimental Psychology. General, 128, 309–331.PubMedCrossRefGoogle Scholar
- Frank, M. J., Moustafa, A. A., Haughey, H. M., Curran, T., & Hutchison, K. E. (2007). Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proceedings of the National Academy of Sciences of the United States of America, 104, 16311–16316.PubMedCrossRefGoogle Scholar
- Gladwin, T. E., Figner, B., Crone, E. A., & Wiers, R. W. (2011). Addiction, adolescence, and the integration of control and motivation. Developmental Cognitive Neuroscience, 1, 364–376.PubMedCrossRefGoogle Scholar
- Greenhill, L. L. (1998). Childhood attention deficit hyperactivity disorder: Pharmacological treatments. In P. E. Nathan & J. Gorman (Eds.), A guide to treatments that work (pp. 42–64). New York: Oxford University Press.Google Scholar
- Hadwin, J. A., Brogan, J., & Stevenson, J. (2005). State anxiety and working memory in children: a test of processing efficiency theory. Educational Psychology, 25, 379–393.CrossRefGoogle Scholar
- Haenlein, M., & Caul, W. F. (1987). Attention deficit disorder with hyperactivity: a specific hypothesis of reward dysfunction. Journal of the American Academy of Child and Adolescent Psychiatry, 26, 356–362.PubMedCrossRefGoogle Scholar
- Huang-Pollock, C. L., Mikami, A. Y., Pfiffner, L., & McBurnett, K. (2007). ADHD subtype differences in motivational responsivity but not inhibitory control: evidence from a reward-based variation of the stop signal paradigm. Journal of Clinical Child and Adolescent Psychology, 36, 127–136.PubMedCrossRefGoogle Scholar
- Kittler, J. E., Menard, W., & Phillips, K. A. (2007). Weight concerns in individuals with body dysmorphic disorder. Eating Behaviors, 8, 115–120.PubMedCrossRefGoogle Scholar
- Klingberg, T., Fernell, E., Olesen, P. J., Johnson, M., Gustafsson, P., Dahlström, et al. (2005). Computerized training of working memory in children with ADHD: a randomized, controlled trial. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 177–186.PubMedCrossRefGoogle Scholar
- Kofler, M. J., Rapport, M. D., Bolden, J., Sarver, D. E., & Raiker, J. S. (2010). ADHD and working memory: the impact of central executive deficits and exceeding storage/rehearsal capacity on observed inattentive behavior. Journal of Abnormal Child Psychology, 38, 149–161.PubMedCrossRefGoogle Scholar
- Kort, W., Compaan, E. L., Bleichrodt, N., Resing, W. C. M., Schittekatte, M., Bosmans, M., et al. (2002). WISC-III NL Handleiding. (Dutch Manual). Amsterdam: NIP.Google Scholar
- Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 44, 377–384.PubMedCrossRefGoogle Scholar
- Mayes, S. D., Calhoun, S. L., Chase, G. A., Mink, D. M., & Stagg, R. E. (2009). ADHD subtypes and co-occurring anxiety, depression, and oppositional-defiant disorder: differences in Gordon diagnostic system and Wechsler working memory and processing speed index scores. Journal of Attention Disorders, 12, 540–550.PubMedCrossRefGoogle Scholar
- Nakamura, K., & Hikosaka, O. (2006). Role of dopamine in the primate caudate nucleus in reward modulation of saccades. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 26, 5360–5369.CrossRefGoogle Scholar
- Nigg, J. T. (2006). What causes ADHD? Understanding what goes wrong and why. New York: Guilford Press.Google Scholar
- Oosterlaan, J., Scheres, A., Antrop, I., Roeyers, H., & Sergeant, J. A. (2000). Vragenlijst voor Gedragsproblemen bij Kinderen (VvGK) (Dutch translation of the DBD Rating Scale). Lisse: Swets & Zeitlinger.Google Scholar
- Pelham, W. E., & Fabiano, G. A. (2008). Evidence-based psychosocial treatment for ADHD: an update. Journal of Clinical Child and Adolescent Psychology, 37, 184–214.PubMedCrossRefGoogle Scholar
- Pelham, W. E., Gnagy, E. M., Greenslade, K. E., & Milich, R. (1992). Teacher rating of DSM-III-R symptoms for disruptive behavior disorders. Journal of Clinical Child Psychology, 8, 259–262.Google Scholar
- Raiker, J. S., Rapport, M. D., Kofler, M. J., & Sarver, D. E. (2012). Objectively-measured impulsivity and attention-deficit/hyperactivity disorder (ADHD): testing competing predictions from the working memory and behavioral inhibition models of ADHD. Journal of Abnormal Child Psychology, 40, 699–713.PubMedCrossRefGoogle Scholar
- Rapport, M. D., Alderson, R. M., Kofler, M. J., Sarver, D. E., Bolden, J., & Sims, V. (2008). Working memory deficits in boys with attention-deficit/hyperactivity disorder (ADHD): the contribution of central executive and subsystem processes. Journal of Abnormal Child Psychology, 36, 825–837.PubMedCrossRefGoogle Scholar
- Rapport, M. D., Bolden, J., Kofler, M. J., Sarver, D. E., Raiker, J. S., & Alderson, R. M. (2009). Hyperactivity in boys with attention-deficit/hyperactivity disorder (ADHD): a ubiquitous core symptom or manifestation of working memory deficits? Journal of Abnormal Child Psychology, 37, 521–534.PubMedCrossRefGoogle Scholar
- Rose, E. J., & Ebmeier, K. P. (2006). Pattern of impaired working memory during major depression. Journal of Affective Disorders, 90, 149–161.PubMedCrossRefGoogle Scholar
- Sarkis, S. M., Sarkis, E. H., Marshall, D., & Archer, J. (2005). Self-regulation and inhibition in comorbid ADHD children: an evaluation of executive functions. Journal of Attention Disorders, 8, 96–108.PubMedCrossRefGoogle Scholar
- Sattler, J. M. (2001). Assessment of children: Cognitive applications (4th ed.). San Diego: Author.Google Scholar
- Schatz, D. B., & Rostain, A. L. (2006). ADHD with comorbid anxiety: a review of the current literature. Journal of Attention Disorders, 10, 141–149.PubMedCrossRefGoogle Scholar
- Scheres, A., Milham, M. P., Knutson, B., & Castellanos, F. X. (2007). Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biological Psychiatry, 61, 720–724.PubMedCrossRefGoogle Scholar
- Scheres, A., Lee, A., & Sumiya, M. (2008). Temporal reward discounting and ADHD: task and symptom specific effects. Journal of Neural Transmission, 115, 221–226.PubMedCrossRefGoogle Scholar
- Sergeant, J. A., Oosterlaan, J., & Van der Meere, J. (1999). Information processing and energetic factors in attention-deficit/hyperactivity disorder. In H. C. Quay & A. E. Hogan (Eds.), Handbook of disruptive behavior disorders (pp. 75–104). New York: Kluwer Academic/Plenum Publishers.CrossRefGoogle Scholar
- Shaffer, D., Fisher, P., Lucas, C. P., Dulcan, M. K., & Schwab-Stone, M. E. (2000). NIMH diagnostic interview schedule for children version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. Journal of the American Academy of Child and Adolescent Psychiatry, 39, 28–38.PubMedCrossRefGoogle Scholar
- Shiels, K., Hawk, L. W., Jr., Lysczek, C. L., Tannock, R., Pelham, W. E., Jr., Spencer, S. V., et al. (2008). The effects of incentives on visual-spatial working memory in children with attention-deficit/hyperactivity disorder. Journal of Abnormal Child Psychology, 36, 903–913.PubMedCrossRefGoogle Scholar
- Sonuga-Barke, E. J. S. (2002). Psychological heterogeneity in AD/HD—a dual pathway model of behaviour and cognition. Behavioral and Brain Research, 130, 29–36.CrossRefGoogle Scholar
- Sonuga-Barke, E. J. S., Sergeant, J. A., Nigg, J. T., & Willcutt, E. G. (2008). Executive dysfunction and delay aversion in ADHD: nosological and diagnostic implications. Child and Adolescent Psychiatric Clinics of North America, 17, 367–384.PubMedCrossRefGoogle Scholar
- Sonuga-Barke, E. J. S., Bitsakou, P., & Thompson, M. (2010). Beyond the dual pathway model: Evidence for the dissociation of timing, inhibitory control, and delay-related impairments in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 49, 345–355.PubMedGoogle Scholar
- Steinberg, L., Albert, D., Cauffman, E., Banich, M., Graham, S., & Woolard, J. (2008). Age differences in sensation seeking and impulsivity as indexed by behavior and self-report: evidence for a dual systems model. Developmental Psychology, 44, 1764–1778.PubMedCrossRefGoogle Scholar
- Strand, M. T., Hawk, L. W., Bubnik, M., Shiels, K., Pelham, W. E., & Waxmonsky, J. G. (2012). Improving working memory in children with attention-deficit/hyperactivity disorder: the separate and combined effects of incentives and stimulant medication. Journal of Abnormal Child Psychology, 40, 1193–1207.PubMedCrossRefGoogle Scholar
- Ströhle, A., Stoy, M., Wrase, J., Schwarzer, S., Schlagenhauf, F., Huss, et al. (2008). Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. NeuroImage, 39, 966–972.PubMedCrossRefGoogle Scholar
- Tillman, C., Eninger, L., Forssman, L., & Bohlin, G. (2011). The relation between working memory components and ADHD symptoms from a developmental perspective. Developmental Neuropsychology, 36, 181–198.PubMedCrossRefGoogle Scholar
- Tripp, G., & Wickens, J. R. (2008). Research review: dopamine transfer deficit: a neurobiological theory of altered reinforcement mechanisms in ADHD. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 49, 691–704.PubMedCrossRefGoogle Scholar
- Van der Meere, J., Hughes, K. A., Börger, N., & Sallee, F. R. (1995). The effect of reward on sustained attention in AD/HD children with and without CD. In J. A. Sergeant (Ed.), European approach to hyperkinetic disorder (pp. 241–253). Zurich: Fotorotar.Google Scholar
- Van der Oord, S., Ponsioen, A. J. G. B., Geurts, H. M., Ten Brink, E. L., & Prins, P. J. M. (2012). A pilot study of the efficacy of a computerized executive functioning remediation training with game elements for children with ADHD in an outpatient setting: outcome on parent- and teacher-rated executive functioning and ADHD behavior. Journal of Attention Disorders. doi: 10.1177/1087054712453167.
- Walsh, N. D., Williams, S. C. R., Brammer, M. J., Bullmore, E. T., Kim, J., Suckling, J., et al. (2007). A longitudinal functional magnetic resonance imaging study of verbal working memory in depression after antidepressant therapy. Biological Psychiatry, 62, 1236–1243.PubMedCrossRefGoogle Scholar
- Wechsler, D. (1958). The measurement and appraisal of adult intelligence (4th ed.). Baltimore: Williams & Witkins.CrossRefGoogle Scholar
- Willcutt, E. G., Doyle, A. E., Nigg, J. T., Faraone, S. V., & Pennington, B. F. (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biological Psychiatry, 57, 1336–1346.PubMedCrossRefGoogle Scholar
- Willcutt, E. G., Nigg, J. T., Pennington, B. F., Solanto, M. V., Rohde, L. A., Tannock, R., et al. (2012). Validity of DSM–IV attention deficit/hyperactivity disorder symptom dimensions and subtypes. Journal of Abnormal Psychology, 121, 991–1010.PubMedCrossRefGoogle Scholar