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Neural Measures of Visual Attention and Suppression As Biomarkers for ADHD- Associated Inattention

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Neural Measures of Visual Attention and Suppression as Biomarkers for ADHD- associated Inattention

Rebecca Elizabeth Townley
PhD

University of York
Psychology August 2019

Abstract

Abstract

Whilst there is a wealth of literature examining neural differences in those with
ADHD, few have investigated visual-associated regions. Given extensive evidence demonstrating visual-attention deficits in ADHD, it is possible that inattention problems may be associated with functional abnormalities within the visual system. By measuring neural responses across the visual system during visual-attentional tasks, we aim to explore the relationship between visual processing and ADHD-associated Inattention in the typically developed population.

We first explored whether differences in neural responses occurred within the superior colliculus (SC); an area linked to distractibility and attention. Here we found that Inattention traits positively correlated with SC activity, but only when distractors were presented in the right visual field (RVF) and not the left visual field (LVF).

Our later work followed up on these findings to investigate separate responses towards task-relevant targets and irrelevant, peripheral distractors. Findings showed that those with High Inattention exhibited increased responses towards distractors compared to targets, while those with Low Inattention showed the opposite effect. Hemifield differences were also observed where those with High Inattention showed increased RVF distractor-related signals compared to those with Low Inattention. No differences were observed for the LVF.

Finally, we examined attention and suppression-related neural responses. Our results indicated that, while attentional responses were similar between Inattention groups, those with High Inattention showed weaker suppression responses towards the unattended RVF. No differences were found when suppressing the LVF.

Findings across all studies suggest that differences in neural responses between those with High and Low levels of Inattention exist within the visual system. Such differences appear to relate to suppression of task-irrelevant distractors rather than attention towards task-relevant targets, suggesting such mechanisms are differentially affected in those with frequent Inattention problems. We also show a clear relationship between Inattention traits and visual suppression of the RVF.

2
Abstract

List of Contents

Abstract................................................................................................................... 2 Abbreviations .......................................................................................................... 6 List of Tables............................................................................................................ 7 List of Figures........................................................................................................... 8 Acknowledgements................................................................................................ 11 Declaration............................................................................................................ 12 Chapter One: Introduction...................................................................................... 13

ADHD Symptoms and Diagnosis criteria..............................................................................13 Diagnostic Tools...................................................................................................................16 Prevalence ...........................................................................................................................18
1.2.1 1.2.2 1.2.3

Sustained attention .............................................................................................................19 Visual field differences in Attention....................................................................................28 Attentional Load ..................................................................................................................32
1.3.1 1.3.2 1.3.3

Functional Differences.........................................................................................................36 Structural Differences..........................................................................................................40 Superior Colliculus ...............................................................................................................43
1.4.1 1.4.2 1.4.3

Chapter Two: Assessing ADHD in the typical population ......................................... 61

2.1 2.2 2.3
Participant Recruitment .................................................................................... 61 Ethics of measuring ADHD ................................................................................. 62 Measuring ADHD traits using the CAARS............................................................ 64

Chapter Three: Evidence for hyperactivity in the superior colliculus in ADHD........... 75

3.1 3.2 3.3
Abstract............................................................................................................ 75 Introduction...................................................................................................... 76 Methodology .................................................................................................... 78

Participants..........................................................................................................................78 Saccade tasks.......................................................................................................................79 Functional imaging: Stimuli and Task..................................................................................81 MRI acquisition....................................................................................................................83 Analyses of MRI data ...........................................................................................................83
3.3.1 3.3.2 3.3.3 3.3.4 3.3.5

Saccade task ........................................................................................................................85 fMRI: Sustained Attention Task and Inattention Traits.......................................................85
3.4.1 3.4.2

3
Abstract

Chapter Four: Characterising Visual EEG responses in Inattention: exploring the effects of Hemifield and Attentional load................................................................ 93

Perceptual Load................................................................................................................... 94 Sensory Competition........................................................................................................... 96 Asymmetrical Spatial Attention .......................................................................................... 96 The Steady State Visual Evoked Potential and its application to research on attention.... 97 Hypotheses and predictions................................................................................................ 99
4.2.1 4.2.2 4.2.3 4.2.4 4.2.5

Participants.......................................................................................................................... 99 EEG Apparatus................................................................................................................... 102 Stimuli and experimental procedure ................................................................................ 102 Eye tracking apparatus and analysis ................................................................................. 106 EEG Analysis ...................................................................................................................... 107
4.3.1 4.3.2 4.3.3 4.3.4 4.3.5

Central target Fixation....................................................................................................... 110 Behavioural Task ............................................................................................................... 111 SSVEP EEG responses ........................................................................................................ 115
4.4.1 4.4.2 4.4.3

Increasing Attentional Load .............................................................................................. 123 Influence of Distractors..................................................................................................... 125 Sensory Competition......................................................................................................... 127 Hemifield ........................................................................................................................... 128 Final Conclusion................................................................................................................. 129
4.5.1 4.5.2 4.5.3 4.5.4 4.5.5

Chapter Five: Examining Cortical and Subcortical visual suppression mechanisms in relation to ADHD.................................................................................................. 131

5.1 5.2 5.3
Abstract...........................................................................................................131 Introduction.....................................................................................................132 Method ...........................................................................................................136

Participants........................................................................................................................ 136 Visual Stimuli ..................................................................................................................... 138 MRI acquisition.................................................................................................................. 141 Defining Regions of Interest.............................................................................................. 141 Behavioural Analysis ......................................................................................................... 142 Blink analysis ..................................................................................................................... 142 MRI analysis....................................................................................................................... 143
5.3.1 5.3.2 5.3.3 5.3.4 5.3.5 5.3.6 5.3.7

Behavioural Accuracy........................................................................................................ 145 Blink events ....................................................................................................................... 146 MRI BOLD Response.......................................................................................................... 148
5.4.1 5.4.2 5.4.3

4
Abstract

Chapter Six: General Discussion.............................................................................167

6.1 6.2 6.3
Overview ........................................................................................................ 167 Summary of Findings....................................................................................... 167 Implications of Results .................................................................................... 170

ADHD and the Visual System.............................................................................................170 Differences in Visual Field Processing ...............................................................................171 Inattention and Suppression Mechanisms........................................................................175 Influence of Distractor Type ..............................................................................................176 Attentional Load ................................................................................................................178
6.3.1 6.3.2 6.3.3 6.3.4 6.3.5

Practical Implications ...................................................................................... 179 Conclusion ...................................................................................................... 180
6.5 6.6

References............................................................................................................182

5
Abbreviations

Abbreviations

  • ADHD
  • Attention-deficit Hyperactivity disorder

ADHD-C ADHD–H ADHD-I
Combined ADHD presentation Hyperactive/Impulsive ADHD presentation Inattention ADHD presentation
ADHD-OS Other specified ADHD ADHD-U ASRS BOLD CAARS CCPT CPT
Unspecified ADHD

Adult self-report scale

Blood Oxygen Level Dependence

Connors Adult ADHD rating scale

Connors’ Continuous performance task Continuous performance task Covert Orienting of Visuospatial Attention Task

Diagnostic and Statistical manual of Mental Disorders

Electroencephalography Functional Magnetic Resonance Imaging Fractional anisotropy
COVAT DSM EEG fMRI FA GNG GM
Go No-go Grey Matter
LGN LVF
Lateral geniculate nucleus Left Visual Field

  • RT
  • Reaction time

RTvar RVF
Reaction time variability Right Visual Field

  • SRT
  • Stimulus response time

  • SC
  • Superior Colliculus

SOA SSVEP VBM VS
Stimulus onset asynchrony Steady-state visual evoked potential Voxel-Based Morphometry Visual search

  • V1
  • Primary visual cortex

  • WM
  • White matter

6
List of Tables

List of Tables

Table 1.1

The 4 main components tested using the Connors Adult ADHD rating scale (CAARS) and examples of associated items (Conners et al., 2002).

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