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The Integration of Bottom-Up and Top THE INTEGRATION OF BOTTOM-UP AND TOP- DOWN SIGNALS IN HUMAN PERCEPTION IN HEALTH AND DISEASE Rimona Sharon Weil Wellcome Trust Centre for Neuroimaging Institute of Cognitive Neuroscience Institute of Neurology University College London Prepared under the supervision of: Professor Geraint Rees Professor Ray Dolan Submitted to UCL for the Degree of PhD 1 DECLARATION I, Rimona Weil, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. The study described in Chapter 5 of this thesis was performed in collaboration with Victoria Wykes. I designed and constructed the stimuli, ran the experiment on some participants, analysed the data and wrote the manuscript which has been submitted for publication by Visual Cognition. The collection of data for the rest of the participants was performed by Victoria Wykes. The study presented in Chapter 7 has been submitted for publication by Cerebral Cortex. The work presented in Chapters 3, 4 and 6 has been published in the following peer reviewed papers: Weil RS, Kilner J, Haynes JD, Rees G. Neural correlates of perceptual filling-in of an artificial scotoma in humans. Proc Natl Acad Sci USA 2007; 104:5211-6. Weil RS, Watkins S and Rees G. Neural correlates of perceptual completion of an artificial scotoma in human visual cortex measured using functional MRI. Neuroimage. 2008;42(4):1519-28 Weil RS, Plant GT, James-Galton M and Rees G. Neural correlates of hemianopic completion across the vertical meridian. Neuropsychologia. 2009;47(2):457-64 2 ACKNOWLEDGEMENTS Above all, I would like to thank my supervisor Geraint Rees. I cannot imagine a more encouraging, supportive and inspiring supervisor, or anyone as able to see the positive in almost any situation. In addition I am grateful to my second supervisor, Ray Dolan, for helpful and timely advice and to Jon Driver for astute input just when it was needed. I would also like to thank the members of the Rees lab – Richard, Su, David, Bahador, Marieke, Chris, Lauri, Ayse, Sharon, Sam, Frank, Claire, Elaine, John and Vic for all their help and advice and for many eventful lab meetings. I would also like to thank many people at the FIL especially the Dolan Group, particularly Mkael Symmonds and Steve Fleming. Also at the FIL, I would like to thank Jenny, Fiona, Bogdan, Nick, Ferath, Guillaume and Jean. Thanks also to the FIL support staff – Peter, Holly, Eric, Marcia, David, Jan, Amanda, Sheila, Kristjan, Gareth, Chris and Rachel. Special thanks to James Kilner for much needed help and support in MEG analysis and to Ric for practical support for a myriad of technical issues Thank you to all the volunteers prepared to lie for many hours in the scanners and special thanks to patient POV for coming back several times to be scanned and always managing to be cheerful. 3 Thanks also to the Medical Research Council for funding me. I would also like to thank my family and friends. In particular, thank you Jonnie, for always asking the questions I don’t have the answers for and being prepared to challenge, inspire and support me. Thank you to Elia and Adina for giving me a sense of perspective. Finally thank you to my parents who always believed in me. 4 ABSTRACT To extract a meaningful visual experience from the information falling on the retina, the visual system must integrate signals from multiple levels. Bottom-up signals provide input relating to local features while top-down signals provide contextual feedback and reflect internal states of the organism. In this thesis I will explore the nature and neural basis of this integration in two key areas. I will examine perceptual filling-in of artificial scotomas to investigate the bottom-up signals causing changes in perception when filling-in takes place. I will then examine how this perceptual filling-in is modified by top-down signals reflecting attention and working memory. I will also investigate hemianopic completion, an unusual form of filling-in, which may reflect a breakdown in top-down feedback from higher visual areas. The second part of the thesis will explore a different form of top-down control of visual processing. While the effects of cognitive mechanisms such as attention on visual processing are well-characterised, other types of top-down signal such as reward outcome are less well explored. I will therefore study whether signals relating to reward can influence visual processing. To address these questions, I will employ a range of methodologies including functional MRI, magnetoencephalography and behavioural testing in healthy participants and patients with cortical damage. I will demonstrate that perceptual filling-in of artificial scotomas is largely a bottom-up process but that higher cognitive 5 functions can modulate the phenomenon. I will also show that reward modulates activity in higher visual areas in the absence of concurrent visual stimulation and that receiving reward leads to enhanced activity in primary visual cortex on the next trial. These findings reveal that integration occurs across multiple levels even for processes rooted in early retinotopic regions, and that higher cognitive processes such as reward can influence the earliest stages of cortical visual processing. 6 CONTENTS Title …………………………………………………………………………... 1 Declaration ……………………………………………………………………. 2 Acknowledgements …………………………………………………………… 3 Abstract ……………………………………………………………………….. 5 Contents ……………………………………………………………………… 7 List of Figures ………………………………………………………………… 17 List of Tables ………………………………………………………………… 20 1. Chapter 1: General Introduction ………………………………………… 21 1.1 Introduction …………………………………………………………. 21 1.1.1 Bottom-up processing: organisation of the visual cortex ……….. 23 1.1.2 Top-down processing of visual information……………………… 24 1.2 Perceptual filling-in………………………………………………… 26 1.2.1 Nomenclature of filling-in………………………………… 27 1.2.2 Current theories of mechanisms of perceptual filling-in…. 28 1.2.3 Previous taxonomies of perceptual filling-in……………… 29 1.2.4 A framework for different forms of perceptual filling-in…. 30 1.2.5 Instant perceptual filling-in dependent on stimulus configuration ……………………………………………………………………. 32 a) Illusory contours ……………..……………………….. 32 b) Illusory surfaces ……………………………………… 37 c) Perceptual filling-in behind occluders: amodal completion ……………………………………………..…………….. 42 1.2.6 Instant perceptual filling-in independent of stimulus configuration …………………………………………………..… 46 7 a) Filling-in at the blind spot…………………………….. 46 b) Filling-in across retinal scotomas……………………… 49 1.2.7 Delayed perceptual filling-in dependent on stimulus configuration ……………………………………………………… 51 a) Troxler fading and artificial scotomas………………….. 51 b) Motion induced blindness……………………………….. 55 1.2.8 Delayed perceptual filling-in independent of stimulus configuration ………………………………………………………. 57 a) Stabilised retinal images……………………………….. 57 1.2.9 Using this framework for perceptual filling-in to explore possible underlying mechanisms………………………………………….. 58 1.2.10 Perceptual filling-in in the context of general perception of contours and surfaces……………………………………….…….. 60 1.3 Reward Influences on visual processing ……………………………................ 63 1.3.1 Processes involved in reward-seeking behaviour………..……….. 63 1.3.1.1 Brain structures involved in representing reward value….. 65 1.3.1.2 Brain structures involved in predicting rewarding events…. 66 1.3.1.3 A dissociation between reward expectation and reward receipt . …………………………………………………………………….. 66 1.3.1.4 Brain structures involved in reward-guided behaviour…… 67 1.3.2 Could reward influence the earliest stages of visual processing? ….. 67 1.4 Summary of studies presented in this thesis……………………….... 69 1.5 Conclusion…………………………………………………………… 71 2. Chapter 2: General methods ……………………………………………….. 73 8 2.1 Introduction …………………………………………………………. 73 2.2 Functional MRI ………………………………………………….….. 73 2.2.1 Physics of MRI …………………………………………….. 73 2.2.2 Formation of images using MRI…………………………….. 76 2.2.3 Contrast ……………………………………………….…….. 77 2.2.4 Echo-planar imaging ………………………………..……….. 78 2.2.5 The basis of the BOLD signal……………………………….. 78 2.2.6 Neural basis of the BOLD signal…………………………….. 80 2.3 fMRI analysis…………………………………………………..…….. 83 2.3.1 Preprocessing………………………………………………... 85 2.3.1.1 Spatial realignment……………………………….. 85 2.3.1.2 Unwarping………………………………………... 86 2.3.1.3 Coregistration to T1 structural image…………….. 86 2.3.1.4 Spatial normalisation………………………….….. 87 2.3.1.5 Spatial smoothing………………………………….. 88 2.3.2 Statistical Parametric Mapping…………………………….. 88 2.3.2.1 Overview…………………………………………. 88 2.3.2.2 General linear model………………………..…….. 89 2.3.2.3 t and F statistics…………………………………….. 91 2.4 Retinotopic mapping………………………………………………….. 92 2.4.1 Retinotopic organisation of visual areas…………………….. 92 2.4.2 Meridian mapping……………………………………..…….. 95 2.4.2.1 Meridian mapping using MrGray………………….. 96 2.4.2.2 Meridian mapping using FreeSurfer …………….. 99 2.5 Magnetoencephalography……………………………….………….. 101 9 2.5.1 Introduction………………………………………………… 101 2.5.2 Neurophsyiological basis of MEG signal………………….. 102 2.5.3 MEG acquisition……………………………….…………….. 104 2.5.3.1 Detection of brain magnetic fields……………….. 104 2.5.3.2 Set-up of the MEG system……………………….. 105 2.5.3.3 Noise reduction……………………………….….. 107 2.5.4 MEG analysis………………………………………………. 108 2.5.4.1 Data acquisition and sampling…………..………… 108 2.5.4.2 Signal processing…………………………………. 108 2.5.4.3 Artefact detection………………………………… 109 2.5.4.4 Event-related fields……………………………….
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