4.7 Article

Neural circuitry underlying sustained attention in healthy adolescents and in ADHD symptomatology

Journal

NEUROIMAGE
Volume 169, Issue -, Pages 395-406

Publisher

ACADEMIC PRESS INC ELSEVIER SCIENCE
DOI: 10.1016/j.neuroimage.2017.12.030

Keywords

Functional connectivity; fMRI; Reaction-time variability; SST; Attention; ADHD

Funding

  1. Irish Research Council [GOIPG/2016/1635, GOIPG/2014/418, GOIPD/2017/798]
  2. China Scholarship Council
  3. Science Foundation Ireland [16/ERCD/3797]
  4. Brain and Behavior Research Foundation [23599, 24065]
  5. National Institute of Mental Health [R03MH104334]
  6. European Union [LSHM-CT-2007-037286]
  7. ERC [695313]
  8. ERANID [PR-ST-0416-10004]
  9. BRIDGET (JPND: BRain Imaging, cognition Dementia and next generation GEnomics) [MR/N027558/1]
  10. FP7 project IMAGEMEND [602450]
  11. FP7 project MATRICS [603016]
  12. Innovative Medicine Initiative Project EU-AIMS [115300-2]
  13. Medical Research Council [MR/N000390/1]
  14. Swedish Research Council Formas
  15. Medical Research Council
  16. National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London
  17. Bundesministeriumfur Bildung und Forschung (BMBF) [01GS08152, 01EV0711, SysAlc01ZX1311A]
  18. Bundesministeriumfur Bildung und Forschung (BMBF Forschungsnetz AERIAL)
  19. Deutsche Forschungsgemeinschaft (DFG) [SM 80/7-1, SM 80/7-2, SFB 940/1]
  20. ANR [AF12-NEUR0008-01 - WM2NA, ANR-12-SAMA-0004]
  21. Fondation de France
  22. Fondation pour la Recherche Medicale
  23. Mission Interministerielle de Lutte-contre-les-Drogues-et-les-Conduites-Addictives (MILDECA)
  24. Fondation pour la Recherche Medicale [DPA20140629802]
  25. Fondation de l'Avenir, Paris-Sud University IDEX
  26. National Institutes of Health, U.S.A. [RO1 MH085772-01A1]
  27. NIH [U54 EB020403]
  28. cross-NIH alliance
  29. Medical Research Council [G0901858] Funding Source: researchfish
  30. NATIONAL INSTITUTE OF BIOMEDICAL IMAGING AND BIOENGINEERING [U54EB020403] Funding Source: NIH RePORTER
  31. NATIONAL INSTITUTE OF MENTAL HEALTH [R03MH104334, R01MH085772] Funding Source: NIH RePORTER
  32. MRC [MR/N000390/1, G0901858] Funding Source: UKRI

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Moment-to-moment reaction time variability on tasks of attention, often quantified by intra-individual response variability (IRV), provides a good indication of the degree to which an individual is vulnerable to lapses in sustained attention. Increased IRV is a hallmark of several disorders of attention, including Attention-Deficit/Hyperactivity Disorder (ADHD). Here, task-based fMRI was used to provide the first examination of how average brain activation and functional connectivity patterns in adolescents are related to individual differences in sustained attention as measured by IRV. We computed IRV in a large sample of adolescents (n = 758) across 'Go' trials of a Stop Signal Task (SST). A data-driven, multi-step analysis approach was used to identify networks associated with low IRV (i.e., good sustained attention) and high IRV (i.e., poorer sustained attention). Low IRV was associated with greater functional segregation (i.e., stronger negative connectivity) amongst an array of brain networks, particularly between cerebellum and motor, cerebellum and prefrontal, and occipital and motor networks. In contrast, high IRV was associated with stronger positive connectivity within the motor network bilaterally and between motor and parietal, prefrontal, and limbic networks. Consistent with these observations, a separate sample of adolescents exhibiting elevated ADHD symptoms had increased fMRI activation and stronger positive connectivity within the same motor network denoting poorer sustained attention, compared to a matched asymptomatic control sample. With respect to the functional connectivity signature of low IRV, there were no statistically significant differences in networks denoting good sustained attention between the ADHD symptom group and asymptomatic control group. We propose that sustained attentional processes are facilitated by an array of neural networks working together, and provide an empirical account of how the functional role of the cerebellum extends to cognition in adolescents. This work highlights the involvement of motor cortex in the integrity of sustained attention, and suggests that atypically strong connectivity within motor networks characterizes poor attentional capacity in both typically developing and ADHD symptomatic adolescents.

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