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Binocular rivalry transitions predict inattention symptom severity in adult ADHD

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Abstract

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.

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References

  1. Polanczyk G, Rohde LA (2007) Epidemiology of attention-deficit/hyperactivity disorder across the lifespan. Curr Opin Psychiatry 20:386–392

    Article  PubMed  Google Scholar 

  2. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Association, Washington, DC

  3. Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94

    Article  PubMed  Google Scholar 

  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 23:729–749

    Article  CAS  Google Scholar 

  5. Shifrin JG, Proctor BE, Prevatt FF (2009) Work performance differences between college students with and without ADHD. J Atten Dis 13:489–496

    Article  Google Scholar 

  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 38:113–128

    Article  Google Scholar 

  7. Posner MI (1995) Attention in cognitive neuroscience: an overview. In: Gazaniga M (ed) The cognitive neuroscience, MIT Press, Cambridge, p 615–624

    Google Scholar 

  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 531–556

    Google Scholar 

  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 115:93–103

    Article  PubMed  PubMed Central  Google Scholar 

  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 45:274–283

    Article  PubMed  Google Scholar 

  11. Barkley RA, Murphy K, Kwasnik D (1996) Psychological adjustment and adaptive impairments in young adults with ADHD. J Atten Dis 1:41–54

    Article  Google Scholar 

  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 35:745–758

    Article  Google Scholar 

  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 115:249–260

    Article  PubMed  CAS  Google Scholar 

  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 101:62–72

    Article  PubMed  Google Scholar 

  15. Lipszyc J, Schacher R (2010) Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. J Int Neuropsych Soc 16:1064–1076

    Article  Google Scholar 

  16. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215

    Article  PubMed  CAS  Google Scholar 

  17. Knudsen EI (2007) Fundamental components of attention. Annu Rev Neurosci 30:57–78

    Article  PubMed  CAS  Google Scholar 

  18. Blake R, Logothetis NK (2002) Visual competition. Nat Revi Neurosci 3:13–21

    Article  CAS  Google Scholar 

  19. Leopold DA, Logothetis NK (1999) Multistable phenomena: changing views in perception. Trends Cogn Sci 3:254–264

    Article  PubMed  CAS  Google Scholar 

  20. Sterzer P, Kleinschmidt A, Rees G (2009) The neural bases of multistable perception. Trends Cogn Sci 13:310–318

    Article  PubMed  Google Scholar 

  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 6:8–8

    Article  Google Scholar 

  22. Klink PC, Brascamp JW, Blake R, van Wezel RJ (2010) Experience-driven plasticity in binocular vision. Curr Biol 20:1464–1469

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Robertson CE, Kravitz DJ, Freyberg J, Baron-Cohen S, Baker CI (2013) Slower rate of binocular rivalry in autism. J Neurosci 33:16983–16991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Robertson CE, Ratai E-M, Kanwisher N (2016) Reduced GABAergic action in the autistic brain. Curr Biol 26:80–85

    Article  PubMed  CAS  Google Scholar 

  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 77:59–66

    Article  PubMed  Google Scholar 

  26. Chong SC, Tadin D, Blake R (2005) Endogenous attention prolongs dominance durations in binocular rivalry. J Vis 5:6–6

    Article  Google Scholar 

  27. Meng M, Tong F (2004) Can attention selectively bias bistable perception? Differences between binocular rivalry and ambiguous figures. J Vis 4:2–2

    Article  Google Scholar 

  28. Paffen CL, Alais D (2011) Attentional modulation of binocular rivalry. Front Hum Neursci 5:105

    Google Scholar 

  29. Alais D, van Boxtel JJ, Parker A, van Ee R (2010) Attending to auditory signals slows visual alternations in binocular rivalry. Vis Res 50:929–935

    Article  PubMed  Google Scholar 

  30. Paffen CL, Alais D, Verstraten FA (2006) Attention speeds binocular rivalry. Psychol Sci 17:752–756

    Article  PubMed  Google Scholar 

  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 31:10293–10301

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Lumer ED, Friston KJ, Rees G (1998) Neural correlates of perceptual rivalry in the human brain. Science 280:1930–1934

    Article  PubMed  CAS  Google Scholar 

  33. Zaretskaya N, Thielscher A, Logothetis NK, Bartels A (2010) Disrupting parietal function prolongs dominance durations in binocular rivalry. Curr Biol 20:2106–2111

    Article  PubMed  CAS  Google Scholar 

  34. Weilnhammer VA, Ludwig K, Hesselmann G, Sterzer P (2013) Frontoparietal cortex mediates perceptual transitions in bistable perception. J Neurosci 33:16009–16015

    Article  PubMed  CAS  Google Scholar 

  35. Carmel D, Walsh V, Lavie N, Rees G (2010) Right parietal TMS shortens dominance durations in binocular rivalry. Curr Biol 20:R799–R800

    Article  PubMed  CAS  Google Scholar 

  36. Kanai R, Bahrami B, Rees G (2010) Human parietal cortex structure predicts individual differences in perceptual rivalry. Curr Biol 20:1626–1630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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–R107

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 169:1038–1055

    Article  Google Scholar 

  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 70:185–198

    Article  PubMed  Google Scholar 

  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 1–12

  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 172:674–683

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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 19:1064–1073

    Article  Google Scholar 

  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 42:16–27

    Article  PubMed  Google Scholar 

  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, Paris

    Google Scholar 

  46. Rösler M, Retz-Junginger P, Retz W, Stieglitz R (2008) HASE–Homburger ADHS-Skalen für Erwachsene. Hogrefe, Göttingen

    Google Scholar 

  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 79:320–327

    Article  PubMed  Google Scholar 

  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 73:830–838

    Article  PubMed  CAS  Google Scholar 

  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 75:888–895

    Article  PubMed  Google Scholar 

  50. Conners C, Ehrhard D, Sparrow D (1999) Conner’s adult ADHD rating scales: CAARS. Multi-Health Systems Incorporated, Toronto

    Google Scholar 

  51. Formann A, Piswanger K (1979) Wiener matrizen-test. Manual. Beltz Test Gesellschaft, Weinheim

    Google Scholar 

  52. Formann A, Waldherr K, Piswanger K (2011) Wiener matrizen-test 2. Manual. Beltz Test GmbH, Göttingen

    Google Scholar 

  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 49:59–69

    Article  PubMed  Google Scholar 

  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 47:2389–2396

    Article  PubMed  PubMed Central  Google Scholar 

  55. Chong SC, Blake R (2006) Exogenous attention and endogenous attention influence initial dominance in binocular rivalry. Vis Res 46:1794–1803

    Article  PubMed  Google Scholar 

  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 23:823–827

    Article  PubMed  CAS  Google Scholar 

  57. Edden RE, Crocetti D, Zhu H, Gilbert DL, Mostofsky SH (2012) Reduced gaba concentration in attention-deficit/hyperactivity disorder. Arch Gen Psychiat 69:750–753

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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 41:410–418

    Article  CAS  Google Scholar 

  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 41:934–941

    Article  PubMed  CAS  Google Scholar 

  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 9:18–18

    Article  PubMed  PubMed Central  Google Scholar 

  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 18:817–827

    Article  PubMed  Google Scholar 

  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 16:1479–1488

    Article  PubMed  CAS  Google Scholar 

  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 21:1146–1161

    Article  Google Scholar 

  64. Halperin JM, Schulz KP (2006) Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder. Psychol Bull 132:560

    Article  PubMed  Google Scholar 

  65. Schoechlin C, Engel RR (2005) Neuropsychological performance in adult attention-deficit hyperactivity disorder: meta-analysis of empirical data. Arch Clin Neuropsychol 20:727–744

    Article  PubMed  Google Scholar 

  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:e589

    Article  CAS  Google Scholar 

  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 26:445–465

    Article  PubMed  PubMed Central  Google Scholar 

  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 11:125–139

    Article  Google Scholar 

  69. Asherson P, Manor I, Huss M (2014) Attention-deficit/hyperactivity disorder in adults: update on clinical presentation and care. Neuropsychiatry 4:109–128

    Article  Google Scholar 

  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:e31500

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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:e0165120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

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.

Funding

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.

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    Authors and Affiliations

    1. LEAD Graduate School and Research Network, University of Tübingen, Gartenstr. 29A, 72074, Tübingen, Germany

      Aiste Jusyte

    2. Department of Psychology, University of Tübingen, Tübingen, Germany

      Aiste Jusyte, Natalia Zaretskaya, Nina Maria Höhnle, Andreas Bartels & Michael Schönenberg

    3. Vision and Cognition Lab, Werner Reichardt Centre for Integrative Neuroscience, Tübingen, Germany

      Natalia Zaretskaya & Andreas Bartels

    4. Max Planck Institute for Biological Cybernetics, Tübingen, Germany

      Natalia Zaretskaya & Andreas Bartels

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    1. Aiste Jusyte
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    Aiste Jusyte and Natalia Zaretskaya contributed equally.

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    Jusyte, A., Zaretskaya, N., Höhnle, N.M. et al. Binocular rivalry transitions predict inattention symptom severity in adult ADHD. Eur Arch Psychiatry Clin Neurosci 268, 373–382 (2018). https://doi.org/10.1007/s00406-017-0790-1

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