Skip to main content

Advertisement

Log in

Brain activation deficit in increased-load working memory tasks among adults with ADHD using fMRI

  • Original Paper
  • Published:
European Archives of Psychiatry and Clinical Neuroscience Aims and scope Submit manuscript

Abstract

Working memory (WM) is impaired among adults with attention-deficit hyperactivity disorder (ADHD). This study aimed to investigate the brain activation deficit for low-level or increased-load WM among adults with ADHD. A total of 20 adults with ADHD and controls were recruited according to diagnostic interviewing by a psychiatrist. Phonological and visual–spatial 2-back and 3-back tasks were performed under functional magnetic resonance scanning. The results demonstrated that both the adults with ADHD and the controls exhibited activation of the fronto-parietal network for WM, and the intensity was greater in the adult ADHD group. The ADHD group had higher brain activation over the bilateral anterior cingulate, left inferior frontal lobe, hippocampus, and supplementary motor area (SMA) for phonological WM than the control group. When the task loading increased from 2-back to 3-back tasks, the adults with ADHD perceived greater difficulty. The control group exhibited increased brain activation over the frontal–parietal network in response to increased phonological WM load. However, the ADHD group showed decreased brain activation over the left precuneus, insula, and SMA. Further analysis demonstrated that the ADHD group exhibited a greater decrease in brain activation over the left fronto-parietal network, including the precuneus, SMA, insula/inferior frontal lobe, and dorsolateral prefrontal cortex, than the control group. These results suggest that adults with ADHD pay more effort to low demanding phonological WM. On the other hand, brain activation of the left fronto-parietal network is impaired when the demands of WM exceed the capacity of adults with ADHD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders, 4th edn, (Text Revision edn). American Psychiatric Association, Washington, DC

  2. de Zwaan M, Gruss B, Müller A, Graap H, Martin A, Glaesmer H, Hilbert A, Philipsen A (2012) The estimated prevalence and correlates of adult ADHD in a German community sample. Eur Arch Psychiatry Clin Neurosci 262(1):79–86

    Article  PubMed  Google Scholar 

  3. Simon V, Czobor P, Bálint S, Mészáros A, Bitter I (2009) Prevalence and correlates of adult attention-deficit hyperactivity disorder: meta-analysis. Br J Psychiatry 194(3):204–211

    Article  PubMed  Google Scholar 

  4. Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005) Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 57(11):1336–1346

    Article  PubMed  Google Scholar 

  5. Müller BW, Gimbel K, Keller-Pliessnig A, Sartory G, Gastpar M, Davids E (2007) Neuropsychological assessment of adult patients with attention-deficit/hyperactivity disorder. Eur Arch Psychiatry Clin Neurosci 257(2):112–119

    Article  PubMed  Google Scholar 

  6. Kofler MJ, Rapport MD, Bolden J, Sarver DE, Raiker JS (2010) ADHD and working memory: the impact of central executive deficits and exceeding storage/rehearsal capacity on observed inattentive behavior. J Abnorm Child Psychol 38(2):149–161

    Article  PubMed  Google Scholar 

  7. Rapport MD, Bolden J, Kofler MJ, Sarver DE, Raiker JS, Alderson RM (2009) Hyperactivity in boys with attention-deficit/hyperactivity disorder (ADHD): a ubiquitous core symptom or manifestation of working memory deficits? J Abnorm Child Psychol 37(4):521–534

    Article  PubMed  Google Scholar 

  8. Baddeley A (2012) Working memory: theories, models, and controversies. Annu Rev Psychol 63:1–29

    Article  PubMed  Google Scholar 

  9. Rapport MD, Alderson RM, Kofler MJ, Sarver DE, Bolden J, Sims V (2008) Working memory deficits in boys with attention-deficit/hyperactivity disorder (ADHD): the contribution of central executive and subsystem processes. J Abnorm Child Psychol 36(6):825–837

    Article  PubMed  Google Scholar 

  10. Aycicegi-Dinn A, Dervent-Ozbek S, Yazgan Y, Bicer D, Dinn WM (2011) Neurocognitive correlates of adult attention-deficit/hyperactivity disorder in a Turkish sample. Atten Defic Hyperact Disord 3(1):41–52

    Article  PubMed  Google Scholar 

  11. Durston S (2003) A review of the biological bases of ADHD: what have we learned from imaging studies? Ment Retard Dev Disabil Res Rev 9(3):184–195

    Article  PubMed  Google Scholar 

  12. Konrad A, Dielentheis TF, El Masri D, Dellani PR, Stoeter P, Vucurevic G, Winterer G (2012) White matter abnormalities and their impact on attentional performance in adult attention-deficit/hyperactivity disorder. Eur Arch Psychiatry Clin Neurosci 262(4):351–360

    Article  PubMed  Google Scholar 

  13. Schweitzer JB, Faber TL, Grafton ST, Tune LE, Hoffman JM, Kilts CD (2000) Alterations in the functional anatomy of working memory in adult attention deficit hyperactivity disorder. Am J Psychiatry 157(2):278–280

    Article  PubMed  CAS  Google Scholar 

  14. Hale TS, Bookheimer S, McGough JJ, Phillips JM, McCracken JT (2007) Atypical brain activation during simple & complex levels of processing in adult ADHD: an fMRI study. J Atten Disord 11(2):125–140

    Article  PubMed  Google Scholar 

  15. Fassbender C, Schweitzer JB, Cortes CR, Tagamets MA, Windsor TA, Reeves GM, Gullapalli R (2011) Working memory in attention deficit/hyperactivity disorder is characterized by a lack of specialization of brain function. PLoS ONE 6(11):e27240

    Article  PubMed  CAS  Google Scholar 

  16. Bayerl M, Dielentheis TF, Vucurevic G, Gesierich T, Vogel F, Fehr C, Stoeter P, Huss M, Konrad A (2010) Disturbed brain activation during a working memory task in drug-naive adult patients with ADHD. NeuroReport 21(6):442–446

    Article  PubMed  Google Scholar 

  17. Valera EM, Faraone SV, Biederman J, Poldrack RA, Seidman LJ (2005) Functional neuroanatomy of working memory in adults with attention-deficit/hyperactivity disorder. Biol Psychiatry 57(5):439–447

    Article  PubMed  Google Scholar 

  18. Martinussen R, Hayden J, Hogg-Johnson S, Tannock R (2005) A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 44(4):377–384

    Article  PubMed  Google Scholar 

  19. Owen AM (2004) Working memory: imaging the magic number four. Curr Biol 14(14):R573–R574

    Article  PubMed  CAS  Google Scholar 

  20. Bolden J, Rapport MD, Raiker JS, Sarver DE, Kofler MJ (2012) Understanding phonological memory deficits in boys with attention-deficit/hyperactivity disorder (ADHD): dissociation of short-term storage and articulatory rehearsal processes. J Abnorm Child Psychol 40(6):999–1011

    Article  PubMed  Google Scholar 

  21. Dige N, Maahr E, Backenroth-Ohsako G (2010) Reduced capacity in a dichotic memory test for adult patients with ADHD. J Atten Disord 13(6):677–683

    Article  PubMed  Google Scholar 

  22. Sörqvist P (2010) The role of working memory capacity in auditory distraction: a review. Noise Health 12(49):217–224

    Article  PubMed  Google Scholar 

  23. Finke K, Schwarzkopf W, Müller U, Frodl T, Müller HJ, Schneider WX, Engel RR, Riedel M, Möller HJ, Hennig-Fast K (2011) Disentangling the adult attention-deficit hyperactivity disorder endophenotype: parametric measurement of attention. J Abnorm Psychol 120(4):890–901

    Article  PubMed  Google Scholar 

  24. Jacob C, Lesch KP (2006) The Wuerzburg Research Initiative on adult attention-deficit/hyperactivity disorder (WURIN-AADHD): multi-layered evaluation of long-term course. Eur Arch Psychiatry Clin Neurosci 256(Suppl 1):i12–i20

    Article  PubMed  Google Scholar 

  25. Callicott JH, Mattay VS, Bertolino A, Finn K, Coppola R, Frank JA, Goldberg TE, Weinberger DR (1999) Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cereb Cortex 9(1):20–26

    Article  PubMed  CAS  Google Scholar 

  26. Linden DE, Bittner RA, Muckli L, Waltz JA, Kriegeskorte N, Goebel R, Singer W, Munk MH (2003) Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network. Neuroimage 20(3):1518–1530

    Article  PubMed  Google Scholar 

  27. Green CT, Long DL, Green D, Iosif AM, Dixon JF, Miller MR, Fassbender C, Schweitzer JB (2012) Will working memory training generalize to improve off-task behavior in children with attention-deficit/hyperactivity disorder? Neurotherapeutics 9(3):639–648

    Article  PubMed  Google Scholar 

  28. Westerberg H, Klingberg T (2007) Changes in cortical activity after training of working memory–a single-subject analysis. Physiol Behav 92(1–2):186–192

    Article  PubMed  CAS  Google Scholar 

  29. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N (1997) Schedule for affective disorders and schizophrenia for school-Age children-present and lifetime version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36(7):980–988

    Article  PubMed  CAS  Google Scholar 

  30. Kessler RC, Adler L, Ames M, Demler O, Faraone S, Hiripi E, Howes MJ, Jin R, Secnik K, Spencer T, Ustun TB, Walters EE (2005) The World Health Organization Adult ADHD Self-Report Scale (ASRS): a short screening scale for use in the general population. Psychol Med 35(2):245–256

    Article  PubMed  Google Scholar 

  31. Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(Suppl 20):22–33 quiz 34–57

    PubMed  Google Scholar 

  32. Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, Noll DC (1997) A parametric study of prefrontal cortex involvement in human working memory. Neuroimage 5(1):49–62

    Article  PubMed  CAS  Google Scholar 

  33. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289

    Google Scholar 

  34. Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3(4):255–274

    Article  PubMed  Google Scholar 

  35. Karlsgodt KH, Shirinyan D, van Erp TG, Cohen MS, Cannon TD (2005) Hippocampal activations during encoding and retrieval in a verbal working memory paradigm. Neuroimage 25(4):1224–1231

    Article  PubMed  Google Scholar 

  36. Duncan J, Owen AM (2000) Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23(10):475–483

    Article  PubMed  CAS  Google Scholar 

  37. Kirschen MP, Chen SH, Schraedley-Desmond P, Desmond JE (2005) Load-and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study. Neuroimage 24(2):462–472

    Article  PubMed  Google Scholar 

  38. Zarahn E, Rakitin B, Abela D, Flynn J, Stern Y (2005) Positive evidence against human hippocampal involvement in working memory maintenance of familiar stimuli. Cereb Cortex 15(3):303–316

    Article  PubMed  Google Scholar 

  39. Brett M, Anton JL, Valabregue R, Poline JB (2002) Region of interest analysis using an SPM toolbox [abstract]. In: Presented at the 8th international conference on functional mapping of the human brain, June 2–6, 2002, Sendai, Japan. Available on CD-ROM in NeuroImage 16

  40. Müller NG, Knight RT (2006) The functional neuroanatomy of working memory: contributions of human brain lesion studies. Neuroscience 139(1):51–58

    Article  PubMed  Google Scholar 

  41. Roth JK, Courtney SM (2007) Neural system for updating object working memory from different sources: sensory stimuli or long-term memory. Neuroimage 38(3):617–630

    Article  PubMed  Google Scholar 

  42. Kaneda M, Osaka N (2008) Role of anterior cingulate cortex during semantic coding in verbal working memory. Neurosci Lett 436(1):57–61

    Article  PubMed  CAS  Google Scholar 

  43. Marvel CL, Desmond JE (2010) The contributions of cerebro-cerebellar circuitry to executive verbal working memory. Cortex 46(7):880–895

    Article  PubMed  Google Scholar 

  44. Oztekin I, McElree B, Staresina BP, Davachi L (2009) Working memory retrieval: contributions of the left prefrontal cortex, the left posterior parietal cortex, and the hippocampus. J Cogn Neurosci 21(3):581–593

    Article  PubMed  Google Scholar 

  45. Izaki Y, Takita M, Akema T (2008) Specific role of the posterior dorsal hippocampus-prefrontal cortex in short-term working memory. Eur J Neurosci 27(11):3029–3034

    Article  PubMed  Google Scholar 

  46. Allen MD, Bigler ED, Larsen J, Goodrich-Hunsaker NJ, Hopkins RO (2007) Functional neuroimaging evidence for high cognitive effort on the Word Memory Test in the absence of external incentives. Brain Inj 21(13–14):1425–1428

    Article  PubMed  Google Scholar 

  47. Honey GD, Fu CH, Kim J, Brammer MJ, Croudace TJ, Suckling J, Pich EM, Williams SC, Bullmore ET (2002) Effects of verbal working memory load on corticocortical connectivity modeled by path analysis of functional magnetic resonance imaging data. Neuroimage 17(2):573–582

    Article  PubMed  CAS  Google Scholar 

  48. Wolf RC, Plichta MM, Sambataro F, Fallgatter AJ, Jacob C, Lesch KP, Herrmann MJ, Schönfeldt-Lecuona C, Connemann BJ, Grön G, Vasic N (2009) Regional brain activation changes and abnormal functional connectivity of the ventrolateral prefrontal cortex during working memory processing in adults with attention-deficit/hyperactivity disorder. Hum Brain Mapp 30(7):2252–2266

    Article  PubMed  Google Scholar 

  49. Duerden EG, Tannock R, Dockstader C (2012) Altered cortical morphology in sensorimotor processing regions in adolescents and adults with attention-deficit/hyperactivity disorder. Brain Res 1445:82–91

    Article  PubMed  CAS  Google Scholar 

  50. O’Hare ED, Lu LH, Houston SM, Bookheimer SY, Sowell ER (2008) Neurodevelopmental changes in verbal working memory load-dependency: an fMRI investigation. Neuroimage 42(4):1678–1685

    Article  PubMed  Google Scholar 

  51. Fusser F, Linden DE, Rahm B, Hampel H, Haenschel C, Mayer JS (2011) Common capacity-limited neural mechanisms of selective attention and spatial working memory encoding. Eur J Neurosci 34(5):827–838

    Article  PubMed  Google Scholar 

  52. Meiron O, Lavidor M (2012) Unilateral prefrontal direct current stimulation effects are modulated by working memory load and gender. Brain Stimul [Epub ahead of print]

  53. Gerton BK, Brown TT, Meyer-Lindenberg A, Kohn P, Holt JL, Olsen RK, Berman KF (2004) Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging. Neuropsychologia 42(13):1781–1787

    Article  PubMed  Google Scholar 

  54. Jones SR, Fernyhough C (2007) Neural correlates of inner speech and auditory verbal hallucinations: a critical review and theoretical integration. Clin Psychol Rev 27(2):140–154

    Article  PubMed  Google Scholar 

  55. Mayer JS, Bittner RA, Nikolić D, Bledowski C, Goebel R, Linden DE (2007) Common neural substrates for visual working memory and attention. Neuroimage 36(2):441–453

    Article  PubMed  Google Scholar 

  56. Dickstein SG, Bannon K, Castellanos FX, Milham MP (2006) The neural correlates of attention deficit hyperactivity disorder: an ALE meta-analysis. J Child Psychol Psychiatry 47(10):1051–1062

    Article  PubMed  Google Scholar 

  57. Palva JM, Monto S, Kulashekhar S, Palva S (2010) Neuronal synchrony reveals working memory networks and predicts individual memory capacity. Proc Natl Acad Sci USA 107(16):7580–7585

    Article  PubMed  CAS  Google Scholar 

  58. Nagel BJ, Ohannessian A, Cummins K (2007) Performance dissociation during verbal and spatial working memory tasks. Percept Mot Skills 105(1):243–250

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the Kaohsiung Municipal Hsiao-Kang Hospital (Kmhk-100-003). The institution has no role in the design, process, analyses, and production of the present study.

Conflict of interest

There is no conflict of interest for the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gin-Chung Liu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (TIFF 235 kb)

Supplementary material 2 (TIFF 6440 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ko, CH., Yen, JY., Yen, CF. et al. Brain activation deficit in increased-load working memory tasks among adults with ADHD using fMRI. Eur Arch Psychiatry Clin Neurosci 263, 561–573 (2013). https://doi.org/10.1007/s00406-013-0407-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00406-013-0407-2

Keywords

Navigation