Binocular rivalry transitions predict inattention symptom severity in adult ADHD

  • Aiste Jusyte
  • Natalia Zaretskaya
  • Nina Maria Höhnle
  • Andreas Bartels
  • Michael Schönenberg
Original Paper


Attention deficit and hyperactivity disorder (ADHD) is a prevalent childhood disorder that is often maintained throughout the development and persists into adulthood. Established etiology models suggest that deficient inhibition underlies the core ADHD symptoms. While experimental evidence for impaired motor inhibition is overwhelming, little is known about the sensory inhibition processes, their changes throughout the development, and the relationship to ADHD symptoms. Here, we used the well-established binocular rivalry (BR) paradigm to investigate for the very first time the inhibitory processes related to visual perception in adults with ADHD. In BR, perception alternates between two dichoptically presented images throughout the viewing period, with shorter dominant percept durations and longer transition periods indicating poorer suppression/inhibition. Healthy controls (N = 28) and patients with ADHD (N = 32) were presented with two dissimilar images (orthogonal gratings) separately to each eye through a mirror stereoscope and asked to report their perceptual experiences. There were no differences between groups in any of the BR markers. However, an association between transition durations and symptom severity emerged in the ADHD group. Importantly, an exploratory multiple regression analysis revealed that inattention symptoms were the sole predictor for the duration of transition periods. The lack of impairments to sensory inhibition in adult, but not pediatric ADHD may reflect compensatory changes associated with development, while a correlation between inhibition and inattention symptoms may reveal an invariant core of the disorder.


Attention deficit and hyperactivity disorder Visual attention Inhibition Binocular rivalry Adults 



The authors would like to thank Mario Kleiner for his assistance with stimulus programming in Psychtoolbox; Alexander Schneidt, and Eva Wiedemann for the support in data collection and Ryan Dutton for language editing.


This research was funded by the German Research Foundation (DFG), Grants No. Scho 1448/2-1, BA4914/1-1, by the Centre for Integrative Neuroscience Tübingen (the German Excellence Initiative of the DFG, grant number EXC307), by the Max Planck Society, Germany, and by the LEAD Graduate School [GSC1028], a project of the Excellence Initiative of the German federal and state governments.

Compliance with ethical standards

Conflict of interest

The authors have no conflict to declare.


  1. 1.
    Polanczyk G, Rohde LA (2007) Epidemiology of attention-deficit/hyperactivity disorder across the lifespan. Curr Opin Psychiatry 20:386–392CrossRefPubMedGoogle Scholar
  2. 2.
    American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Association, Washington, DCGoogle Scholar
  3. 3.
    Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94CrossRefPubMedGoogle Scholar
  4. 4.
    Hart EL, Lahey BB, Loeber R, Applegate B, Frick PJ (1995) Developmental change in attention-deficit hyperactivity disorder in boys: a four-year longitudinal study. J Abnorml Child Psychol 23:729–749CrossRefGoogle Scholar
  5. 5.
    Shifrin JG, Proctor BE, Prevatt FF (2009) Work performance differences between college students with and without ADHD. J Atten Dis 13:489–496CrossRefGoogle Scholar
  6. 6.
    Barkley RA, Cox D (2007) A review of driving risks and impairments associated with attention-deficit/hyperactivity disorder and the effects of stimulant medication on driving performance. J Saf Res 38:113–128CrossRefGoogle Scholar
  7. 7.
    Posner MI (1995) Attention in cognitive neuroscience: an overview. In: Gazaniga M (ed) The cognitive neuroscience, MIT Press, Cambridge, p 615–624Google Scholar
  8. 8.
    Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bouwhuis D (ed) Attention and performance X: control of language processes, Lawrence Erlbaum Associates, Hillsdale, p 531–556Google Scholar
  9. 9.
    Friedman-Hill SR, Wagman MR, Gex SE, Pine DS, Leibenluft E, Ungerleider LG (2010) What does distractibility in ADHD reveal about mechanisms for top-down attentional control? Cognition 115:93–103CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Sonuga-Barke EJ, Houwer JD, Ruiter KD, Ajzenstzen M, Holland S (2004) AD/HD and the capture of attention by briefly exposed delay-related cues: evidence from a conditioning paradigm. J Child Psychol Psychiat 45:274–283CrossRefPubMedGoogle Scholar
  11. 11.
    Barkley RA, Murphy K, Kwasnik D (1996) Psychological adjustment and adaptive impairments in young adults with ADHD. J Atten Dis 1:41–54CrossRefGoogle Scholar
  12. 12.
    Alderson RM, Rapport MD, Kofler MJ (2007) Attention-deficit/hyperactivity disorder and behavioral inhibition: a meta-analytic review of the stop-signal paradigm. J Abnorml Child Psychol 35:745–758CrossRefGoogle Scholar
  13. 13.
    Rommelse N, Van der Stigchel S, Witlox J, Geldof C, Deijen J-B, Theeuwes J, Oosterlaan J, Sergeant J (2008) Deficits in visuo-spatial working memory, inhibition and oculomotor control in boys with ADHD and their non-affected brothers. J Neural Transm 115:249–260CrossRefPubMedGoogle Scholar
  14. 14.
    Fried M, Tsitsiashvili E, Bonneh YS, Sterkin A, Wygnanski-Jaffe T, Epstein T, Polat U (2014) ADHD subjects fail to suppress eye blinks and microsaccades while anticipating visual stimuli but recover with medication. Vision Res 101:62–72CrossRefPubMedGoogle Scholar
  15. 15.
    Lipszyc J, Schacher R (2010) Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. J Int Neuropsych Soc 16:1064–1076CrossRefGoogle Scholar
  16. 16.
    Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215CrossRefPubMedGoogle Scholar
  17. 17.
    Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 30:57–78CrossRefPubMedGoogle Scholar
  18. 18.
    Blake R, Logothetis NK (2002) Visual competition. Nat Revi Neurosci 3:13–21CrossRefGoogle Scholar
  19. 19.
    Leopold DA, Logothetis NK (1999) Multistable phenomena: changing views in perception. Trends Cogn Sci 3:254–264CrossRefPubMedGoogle Scholar
  20. 20.
    Sterzer P, Kleinschmidt A, Rees G (2009) The neural bases of multistable perception. Trends Cogn Sci 13:310–318CrossRefPubMedGoogle Scholar
  21. 21.
    Brascamp JW, van Ee R, Noest AJ, Jacobs RHAH, van den Berg AV (2006) The time course of binocular rivalry reveals a fundamental role of noise. J Vis 6:8–8CrossRefGoogle Scholar
  22. 22.
    Klink PC, Brascamp JW, Blake R, van Wezel RJ (2010) Experience-driven plasticity in binocular vision. Curr Biol 20:1464–1469CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Robertson CE, Kravitz DJ, Freyberg J, Baron-Cohen S, Baker CI (2013) Slower rate of binocular rivalry in autism. J Neurosci 33:16983–16991CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Robertson CE, Ratai E-M, Kanwisher N (2016) Reduced GABAergic action in the autistic brain. Curr Biol 26:80–85CrossRefPubMedGoogle Scholar
  25. 25.
    Said CP, Egan RD, Minshew NJ, Behrmann M, Heeger DJ (2013) Normal binocular rivalry in autism: implications for the excitation/inhibition imbalance hypothesis. Vis Res 77:59–66CrossRefPubMedGoogle Scholar
  26. 26.
    Chong SC, Tadin D, Blake R (2005) Endogenous attention prolongs dominance durations in binocular rivalry. J Vis 5:6–6CrossRefGoogle Scholar
  27. 27.
    Meng M, Tong F (2004) Can attention selectively bias bistable perception? Differences between binocular rivalry and ambiguous figures. J Vis 4:2–2CrossRefGoogle Scholar
  28. 28.
    Paffen CL, Alais D (2011) Attentional modulation of binocular rivalry. Front Hum Neursci 5:105Google Scholar
  29. 29.
    Alais D, van Boxtel JJ, Parker A, van Ee R (2010) Attending to auditory signals slows visual alternations in binocular rivalry. Vis Res 50:929–935CrossRefPubMedGoogle Scholar
  30. 30.
    Paffen CL, Alais D, Verstraten FA (2006) Attention speeds binocular rivalry. Psychol Sci 17:752–756CrossRefPubMedGoogle Scholar
  31. 31.
    Knapen T, Brascamp J, Pearson J, van Ee R, Blake R (2011) The role of frontal and parietal brain areas in bistable perception. J Neurosci 31:10293–10301CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Lumer ED, Friston KJ, Rees G (1998) Neural correlates of perceptual rivalry in the human brain. Science 280:1930–1934CrossRefPubMedGoogle Scholar
  33. 33.
    Zaretskaya N, Thielscher A, Logothetis NK, Bartels A (2010) Disrupting parietal function prolongs dominance durations in binocular rivalry. Curr Biol 20:2106–2111CrossRefPubMedGoogle Scholar
  34. 34.
    Weilnhammer VA, Ludwig K, Hesselmann G, Sterzer P (2013) Frontoparietal cortex mediates perceptual transitions in bistable perception. J Neurosci 33:16009–16015CrossRefPubMedGoogle Scholar
  35. 35.
    Carmel D, Walsh V, Lavie N, Rees G (2010) Right parietal TMS shortens dominance durations in binocular rivalry. Curr Biol 20:R799–R800CrossRefPubMedGoogle Scholar
  36. 36.
    Kanai R, Bahrami B, Rees G (2010) Human parietal cortex structure predicts individual differences in perceptual rivalry. Curr Biol 20:1626–1630CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kanai R, Carmel D, Bahrami B, Rees G (2011) Structural and functional fractionation of right superior parietal cortex in bistable perception. Curr Biol 21:R106–R107CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Cortese S, Kelly C, Chabernaud C, Proal E, Di Martino A, Milham MP, Castellanos FX (2012) Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. Am J Psychat 169:1038–1055CrossRefGoogle Scholar
  39. 39.
    Hart H, Radua J, Nakao T, Mataix-Cols D, Rubia K (2013) Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects. JAMA Psychiatry 70:185–198CrossRefPubMedGoogle Scholar
  40. 40.
    Bollmann S, Ghisleni C, Poil S-S, Martin E, Ball J, Eich-Höchli D, Klaver P, O’Gorman RL, Michels L, Brandeis D (2015) Age-dependent and -independent changes in attention-deficit/hyperactivity disorder (ADHD) during spatial working memory performance. World J Biol Psychiat 1–12Google Scholar
  41. 41.
    Rooij DV, Hoekstra PJ, Mennes M, Rhein DV, Thissen AJAM, Heslenfeld D, Zwiers MP, Faraone SV, Oosterlaan J, Franke B, Rommelse N, Buitelaar JK, Hartman CA (2015) Distinguishing adolescents With ADHD from their unaffected siblings and healthy comparison subjects by neural activation patterns during response inhibition. Am J Psychat 172:674–683CrossRefGoogle Scholar
  42. 42.
    Amador-Campos JA, Aznar-Casanova JA, Moreno-Sánchez M, Medina-Peña A, Ortiz-Guerra JJ (2013) Psychometric properties of a test for ADHD based on binocular rivalry. Spanish J Psychol 16:E20 (8 pages)CrossRefGoogle Scholar
  43. 43.
    Amador-Campos JA, Aznar-Casanova JA, Ortiz-Guerra JJ, Moreno-Sanchez M, Medina-Pena A (2015) Assessing Attention deficit by binocular rivalry. J Attention Dis 19:1064–1073CrossRefGoogle Scholar
  44. 44.
    Aznar-Casanova JA, Amador-Campos JA, Sánchez MM, Supèr H (2013) Onset time of binocular rivalry and duration of inter-dominance periods as psychophysical markers of ADHD. Perception 42:16–27CrossRefPubMedGoogle Scholar
  45. 45.
    Lecrubier Y, Weiller E, Hergueta T, Amorim P, Bonora L, Lépine J, Sheehan D, Janavs J, Baker R, Sheehan K (1998) MINI mini internationales neuropsychiatrisches interview, deutsche version 5.0. 0, DSM-IV & ICD-10. Hôpital de la Salpétrière, ParisGoogle Scholar
  46. 46.
    Rösler M, Retz-Junginger P, Retz W, Stieglitz R (2008) HASE–Homburger ADHS-Skalen für Erwachsene. Hogrefe, GöttingenGoogle Scholar
  47. 47.
    Rösler M, Retz W, Retz-Junginger P, Stieglitz RD, Kessler H, Reimherr F, Wender PH (2008) Attention deficit hyperactivity disorder in adults. Der Nervenarzt 79:320–327CrossRefPubMedGoogle Scholar
  48. 48.
    Retz-Junginger P, Retz W, Blocher D, Weijers H-G, Trott G-E, Wender P, Rössler M (2002) Wender utah rating scale (WURS-k) Die deutsche Kurzform zur retrospektiven Erfassung des hyperkinetischen Syndroms bei Erwachsenen. Der Nervenarzt 73:830–838CrossRefPubMedGoogle Scholar
  49. 49.
    Rösler M, Retz W, Retz-Junginger P, Thome J, Supprian T, Nissen T, Stieglitz R-D, Blocher D, Hengesch G, Trott G (2004) Instrumente zur Diagnostik der Aufmerksamkeitsdefizit-/Hyperaktivitätsstörung (ADHS) im Erwachsenenalter. Der Nervenarzt 75:888–895CrossRefPubMedGoogle Scholar
  50. 50.
    Conners C, Ehrhard D, Sparrow D (1999) Conner’s adult ADHD rating scales: CAARS. Multi-Health Systems Incorporated, TorontoGoogle Scholar
  51. 51.
    Formann A, Piswanger K (1979) Wiener matrizen-test. Manual. Beltz Test Gesellschaft, WeinheimGoogle Scholar
  52. 52.
    Formann A, Waldherr K, Piswanger K (2011) Wiener matrizen-test 2. Manual. Beltz Test GmbH, GöttingenGoogle Scholar
  53. 53.
    Kofler MJ, Rapport MD, Matt Alderson R (2008) Quantifying ADHD classroom inattentiveness, its moderators, and variability: a meta-analytic review. J Child Psychol Psychiat 49:59–69CrossRefPubMedGoogle Scholar
  54. 54.
    Vaurio RG, Simmonds DJ, Mostofsky SH (2009) Increased intra-individual reaction time variability in attention-deficit/hyperactivity disorder across response inhibition tasks with different cognitive demands. Neuropsychologia 47:2389–2396CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Chong SC, Blake R (2006) Exogenous attention and endogenous attention influence initial dominance in binocular rivalry. Vis Res 46:1794–1803CrossRefPubMedGoogle Scholar
  56. 56.
    van Loon AM, Knapen T, Scholte HS, John-Saaltink ES, Donner TH, Lamme VA (2013) GABA shapes the dynamics of bistable perception. Curr Biol 23:823–827CrossRefPubMedGoogle Scholar
  57. 57.
    Edden RE, Crocetti D, Zhu H, Gilbert DL, Mostofsky SH (2012) Reduced gaba concentration in attention-deficit/hyperactivity disorder. Arch Gen Psychiat 69:750–753CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Ende G, Cackowski S, Van Eijk J, Sack M, Demirakca T, Kleindienst N, Bohus M, Sobanski E, Krause-Utz A, Schmahl C (2016) Impulsivity and aggression in female BPD and ADHD patients: association with ACC glutamate and GABA concentrations. Neuropsychopharmacol 41:410–418CrossRefGoogle Scholar
  59. 59.
    Perlov E, Philipsen A, Hesslinger B, Buechert M, Ahrendts J, Feige B, Bubl E, Hennig J, Ebert D, Tebartz van Elst L (2007) Reduced cingulate glutamate/glutamine-to-creatine ratios in adult patients with attention deficit/hyperactivity disorder–a magnet resonance spectroscopy study. J Psychiat Res 41:934–941CrossRefPubMedGoogle Scholar
  60. 60.
    Lauritzen TZ, D’Esposito M, Heeger DJ, Silver MA (2009) Top–down flow of visual spatial attention signals from parietal to occipital cortex. J Vis 9:18–18CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Ruff CC, Bestmann S, Blankenburg F, Bjoertomt O, Josephs O, Weiskopf N, Deichmann R, Driver J (2008) Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS–fMRI. Cereb Cortex 18:817–827CrossRefPubMedGoogle Scholar
  62. 62.
    Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Freeman E, Haynes J-D, Rees G, Josephs O, Deichmann R, Driver J (2006) Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol 16:1479–1488CrossRefPubMedGoogle Scholar
  63. 63.
    Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Weiskopf N, Driver J (2009) Hemispheric differences in frontal and parietal influences on human occipital cortex: direct confirmation with concurrent TMS–fMRI. J Cog Neurosci 21:1146–1161CrossRefGoogle Scholar
  64. 64.
    Halperin JM, Schulz KP (2006) Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder. Psychol Bull 132:560CrossRefPubMedGoogle Scholar
  65. 65.
    Schoechlin C, Engel RR (2005) Neuropsychological performance in adult attention-deficit hyperactivity disorder: meta-analysis of empirical data. Arch Clin Neuropsychol 20:727–744CrossRefPubMedGoogle Scholar
  66. 66.
    Bollmann S, Ghisleni C, Poil SS, Martin E, Ball J, Eich-Hochli D, Edden RAE, Klaver P, Michels L, Brandeis D, O’Gorman RL (2015) Developmental changes in gamma-aminobutyric acid levels in attention-deficit/hyperactivity disorder. Trans Psychiat 5:e589CrossRefGoogle Scholar
  67. 67.
    Fassbender C, Schweitzer JB (2006) Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature. Clin Psychol Rev 26:445–465CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    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 Dis 11:125–139CrossRefGoogle Scholar
  69. 69.
    Asherson P, Manor I, Huss M (2014) Attention-deficit/hyperactivity disorder in adults: update on clinical presentation and care. Neuropsychiatry 4:109–128CrossRefGoogle Scholar
  70. 70.
    Das D, Cherbuin N, Butterworth P, Anstey KJ, Easteal S (2012) A population-based study of attention deficit/hyperactivity disorder symptoms and associated impairment in middle-aged adults. PLoS one 7:e31500CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Sokolova E, Groot P, Claassen T, van Hulzen KJ, Glennon JC, Franke B, Heskes T, Buitelaar J (2016) Statistical evidence suggests that inattention drives hyperactivity/impulsivity in attention deficit-hyperactivity disorder. PLoS one 11:e0165120CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Aiste Jusyte
    • 1
    • 2
  • Natalia Zaretskaya
    • 2
    • 3
    • 4
  • Nina Maria Höhnle
    • 2
  • Andreas Bartels
    • 2
    • 3
    • 4
  • Michael Schönenberg
    • 2
  1. 1.LEAD Graduate School and Research NetworkUniversity of TübingenTübingenGermany
  2. 2.Department of PsychologyUniversity of TübingenTübingenGermany
  3. 3.Vision and Cognition Lab, Werner Reichardt Centre for Integrative NeuroscienceTübingenGermany
  4. 4.Max Planck Institute for Biological CyberneticsTübingenGermany

Personalised recommendations