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

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 <a href="#2_0">Abstract................................................................................................................... 2 </a><a href="#6_0">Abbreviations .......................................................................................................... 6 </a><a href="#7_0">List of Tables............................................................................................................ 7 </a><a href="#8_0">List of Figures........................................................................................................... 8 </a><a href="#11_0">Acknowledgements................................................................................................ 11 </a><a href="#12_0">Declaration............................................................................................................ 12 </a><a href="#13_0">Chapter One: Introduction...................................................................................... 13 </a><ul style="display: flex;"><li style="flex:1"><a href="#13_1">1.1 </a></li><li style="flex:1"><a href="#13_1">Overview .......................................................................................................... 13 </a></li></ul><ul style="display: flex;"><li style="flex:1"><a href="#13_2">1.2 </a></li><li style="flex:1"><a href="#13_2">Attention Deficit Hyperactivity Disorder ............................................................ 13 </a></li></ul><a href="#13_3">ADHD Symptoms and Diagnosis criteria..............................................................................13 </a><a href="#16_0">Diagnostic Tools...................................................................................................................16 </a><a href="#18_0">Prevalence ...........................................................................................................................18 </a> <a href="#13_3">1.2.1 </a><a href="#16_0">1.2.2 </a><a href="#18_0">1.2.3 </a><ul style="display: flex;"><li style="flex:1"><a href="#19_0">1.3 </a></li><li style="flex:1"><a href="#19_0">Visual Attention in ADHD .................................................................................. 19 </a></li></ul><a href="#19_1">Sustained attention .............................................................................................................19 </a><a href="#0_0">Visual field differences in Attentio</a><a href="#0_0">n</a><a href="#0_0">.</a><a href="#0_0">...................................................................................28 </a><a href="#0_1">Attentional Load ..................................................................................................................32 </a> <a href="#19_1">1.3.1 </a><a href="#0_0">1.3.2 </a><a href="#0_1">1.3.3 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_2">1.4 </a></li><li style="flex:1"><a href="#0_2">The Visual System and ADHD............................................................................. 35 </a></li></ul><a href="#0_3">Functional Differences.........................................................................................................36 </a><a href="#0_4">Structural Differences..........................................................................................................40 </a><a href="#0_5">Superior Colliculus ...............................................................................................................43 </a> <a href="#0_3">1.4.1 </a><a href="#0_4">1.4.2 </a><a href="#0_5">1.4.3 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_6">1.5 </a></li><li style="flex:1"><a href="#0_6">Concluding Remarks.......................................................................................... 57 </a></li></ul><a href="#0_7">Chapter Two: Assessing ADHD in the typical population ......................................... 61 </a><a href="#0_8">2.1 </a><a href="#0_9">2.2 </a><a href="#0_10">2.3 </a> <a href="#0_8">Participant Recruitment .................................................................................... 61 </a><a href="#0_9">Ethics of measuring ADHD ................................................................................. 62 </a><a href="#0_10">Measuring ADHD traits using the CAAR</a><a href="#0_10">S</a><a href="#0_10">.</a><a href="#0_10">........................................................... 64 </a><a href="#0_6">Chapter Three: Evidence for hyperactivity in the superior colliculus in ADH</a><a href="#0_6">D</a><a href="#0_6">.</a><a href="#0_6">.......... 75 </a><a href="#0_11">3.1 </a><a href="#0_10">3.2 </a><a href="#0_10">3.3 </a> <a href="#0_11">Abstract............................................................................................................ 75 </a><a href="#0_10">Introduction...................................................................................................... 76 </a><a href="#0_10">Methodology .................................................................................................... 78 </a><a href="#0_12">Participant</a><a href="#0_12">s</a><a href="#0_12">.</a><a href="#0_12">.........................................................................................................................78 </a><a href="#0_2">Saccade task</a><a href="#0_2">s</a><a href="#0_2">.</a><a href="#0_2">......................................................................................................................79 </a><a href="#0_13">Functional imaging: Stimuli and Tas</a><a href="#0_13">k</a><a href="#0_13">.</a><a href="#0_13">.................................................................................81 </a><a href="#0_14">MRI acquisitio</a><a href="#0_14">n</a><a href="#0_14">.</a><a href="#0_14">...................................................................................................................83 </a><a href="#0_15">Analyses of MRI data ...........................................................................................................83 </a> <a href="#0_12">3.3.1 </a><a href="#0_2">3.3.2 </a><a href="#0_13">3.3.3 </a><a href="#0_14">3.3.4 </a><a href="#0_15">3.3.5 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_16">3.4 </a></li><li style="flex:1"><a href="#0_16">Results.............................................................................................................. 85 </a></li></ul><a href="#0_17">Saccade task ........................................................................................................................85 </a><a href="#0_18">fMRI: Sustained Attention Task and Inattention Traits.......................................................85 </a> <a href="#0_17">3.4.1 </a><a href="#0_18">3.4.2 </a>3 Abstract <ul style="display: flex;"><li style="flex:1"><a href="#0_19">3.4.3 </a></li><li style="flex:1"><a href="#0_19">fMRI: Superior colliculus and Inattention ........................................................................... 86 </a></li></ul><ul style="display: flex;"><li style="flex:1"><a href="#0_6">3.5 </a></li><li style="flex:1"><a href="#0_6">Discussion......................................................................................................... 89 </a></li></ul><a href="#0_6">Chapter Four: Characterising Visual EEG responses in Inattention: exploring the </a><a href="#0_6">effects of Hemifield and Attentional load</a><a href="#0_6">.</a><a href="#0_6">............................................................... 93 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_11">4.1 </a></li><li style="flex:1"><a href="#0_11">Abstract............................................................................................................ 93 </a></li></ul><ul style="display: flex;"><li style="flex:1"><a href="#0_20">4.2 </a></li><li style="flex:1"><a href="#0_20">Introduction...................................................................................................... 94 </a></li></ul><a href="#0_21">Perceptual Load................................................................................................................... 94 </a><a href="#0_22">Sensory Competitio</a><a href="#0_22">n</a><a href="#0_22">.</a><a href="#0_22">.......................................................................................................... 96 </a><a href="#0_23">Asymmetrical Spatial Attention .......................................................................................... 96 </a><a href="#0_24">The Steady State Visual Evoked Potential and its application to research on attention.... 97 </a><a href="#0_25">Hypotheses and predictions................................................................................................ 99 </a> <a href="#0_21">4.2.1 </a><a href="#0_22">4.2.2 </a><a href="#0_23">4.2.3 </a><a href="#0_24">4.2.4 </a><a href="#0_25">4.2.5 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_26">4.3 </a></li><li style="flex:1"><a href="#0_26">Method</a><a href="#0_26">s</a><a href="#0_26">.</a><a href="#0_26">.......................................................................................................... 99 </a></li></ul><a href="#0_27">Participants.......................................................................................................................... 99 </a><a href="#0_22">EEG Apparatus................................................................................................................... 102 </a><a href="#0_28">Stimuli and experimental procedure ................................................................................ 102 </a><a href="#0_29">Eye tracking apparatus and analysis ................................................................................. 106 </a><a href="#0_30">EEG Analysis ...................................................................................................................... 107 </a> <a href="#0_27">4.3.1 </a><a href="#0_22">4.3.2 </a><a href="#0_28">4.3.3 </a><a href="#0_29">4.3.4 </a><a href="#0_30">4.3.5 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_31">4.4 </a></li><li style="flex:1"><a href="#0_31">Results.............................................................................................................110 </a></li></ul><a href="#0_32">Central target Fixation....................................................................................................... 110 </a><a href="#0_14">Behavioural Task ............................................................................................................... 111 </a><a href="#0_33">SSVEP EEG responses ........................................................................................................ 115 </a> <a href="#0_32">4.4.1 </a><a href="#0_14">4.4.2 </a><a href="#0_33">4.4.3 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_6">4.5 </a></li><li style="flex:1"><a href="#0_6">Discussion........................................................................................................123 </a></li></ul><a href="#0_34">Increasing Attentional Load .............................................................................................. 123 </a><a href="#0_35">Influence of Distractor</a><a href="#0_35">s</a><a href="#0_35">.</a><a href="#0_35">.................................................................................................... 125 </a><a href="#0_36">Sensory Competitio</a><a href="#0_36">n</a><a href="#0_36">.</a><a href="#0_36">........................................................................................................ 127 </a><a href="#0_37">Hemifield ........................................................................................................................... 128 </a><a href="#0_38">Final Conclusion................................................................................................................. 129 </a> <a href="#0_34">4.5.1 </a><a href="#0_35">4.5.2 </a><a href="#0_36">4.5.3 </a><a href="#0_37">4.5.4 </a><a href="#0_38">4.5.5 </a><a href="#0_6">Chapter Five: Examining Cortical and Subcortical visual suppression mechanisms in </a><a href="#0_6">relation to ADHD</a><a href="#0_6">.</a><a href="#0_6">.</a><a href="#0_6">................................................................................................ 131 </a><a href="#0_39">5.1 </a><a href="#0_22">5.2 </a><a href="#0_40">5.3 </a> <a href="#0_39">Abstract...........................................................................................................131 </a><a href="#0_22">Introduction.....................................................................................................132 </a><a href="#0_40">Method ...........................................................................................................136 </a><a href="#0_21">Participants........................................................................................................................ 136 </a><a href="#0_41">Visual Stimuli ..................................................................................................................... 138 </a><a href="#0_42">MRI acquisition.................................................................................................................. 141 </a><a href="#0_43">Defining Regions of Interest.............................................................................................. 141 </a><a href="#0_44">Behavioural Analysis ......................................................................................................... 142 </a><a href="#0_45">Blink analysis ..................................................................................................................... 142 </a><a href="#0_46">MRI analysis....................................................................................................................... 143 </a> <a href="#0_21">5.3.1 </a><a href="#0_41">5.3.2 </a><a href="#0_42">5.3.3 </a><a href="#0_43">5.3.4 </a><a href="#0_44">5.3.5 </a><a href="#0_45">5.3.6 </a><a href="#0_46">5.3.7 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_6">5.4 </a></li><li style="flex:1"><a href="#0_6">Results.............................................................................................................145 </a></li></ul><a href="#0_47">Behavioural Accurac</a><a href="#0_47">y</a><a href="#0_47">.</a><a href="#0_47">....................................................................................................... 145 </a><a href="#0_48">Blink events ....................................................................................................................... 146 </a><a href="#0_49">MRI BOLD Response.......................................................................................................... 148 </a> <a href="#0_47">5.4.1 </a><a href="#0_48">5.4.2 </a><a href="#0_49">5.4.3 </a>4 Abstract <ul style="display: flex;"><li style="flex:1"><a href="#0_7">5.5 </a></li><li style="flex:1"><a href="#0_7">Discussion....................................................................................................... 161 </a></li></ul><a href="#0_6">Chapter Six: General Discussion.............................................................................167 </a><a href="#0_50">6.1 </a><a href="#0_51">6.2 </a><a href="#0_52">6.3 </a> <a href="#0_50">Overview ........................................................................................................ 167 </a><a href="#0_51">Summary of Findings....................................................................................... 167 </a><a href="#0_52">Implications of Results .................................................................................... 170 </a><a href="#0_53">ADHD and the Visual System.............................................................................................170 </a><a href="#0_54">Differences in Visual Field Processing ...............................................................................171 </a><a href="#0_55">Inattention and Suppression Mechanism</a><a href="#0_55">s</a><a href="#0_55">.</a><a href="#0_55">.......................................................................175 </a><a href="#0_56">Influence of Distractor Type ..............................................................................................176 </a><a href="#0_10">Attentional Load ................................................................................................................178 </a> <a href="#0_53">6.3.1 </a><a href="#0_54">6.3.2 </a><a href="#0_55">6.3.3 </a><a href="#0_56">6.3.4 </a><a href="#0_10">6.3.5 </a><ul style="display: flex;"><li style="flex:1"><a href="#0_57">6.4 </a></li><li style="flex:1"><a href="#0_57">Limitations and Future Direction</a><a href="#0_57">s</a><a href="#0_57">.</a><a href="#0_57">................................................................... 178 </a></li></ul><a href="#0_58">Practical Implications ...................................................................................... 179 </a><a href="#0_59">Conclusion ...................................................................................................... 180 </a> <a href="#0_58">6.5 </a><a href="#0_59">6.6 </a><a href="#0_10">Reference</a><a href="#0_10">s</a><a href="#0_10">............................................................................................................182 </a>5 Abbreviations Abbreviations <ul style="display: flex;"><li style="flex:1">ADHD </li><li style="flex:1">Attention-deficit Hyperactivity disorder </li></ul>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 <ul style="display: flex;"><li style="flex:1">RT </li><li style="flex:1">Reaction time </li></ul>RTvar RVF Reaction time variability Right Visual Field <ul style="display: flex;"><li style="flex:1">SRT </li><li style="flex:1">Stimulus response time </li></ul><ul style="display: flex;"><li style="flex:1">SC </li><li style="flex:1">Superior Colliculus </li></ul>SOA SSVEP VBM VS Stimulus onset asynchrony Steady-state visual evoked potential Voxel-Based Morphometry Visual search <ul style="display: flex;"><li style="flex:1">V1 </li><li style="flex:1">Primary visual cortex </li></ul><ul style="display: flex;"><li style="flex:1">WM </li><li style="flex:1">White matter </li></ul>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).

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

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