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«Richard Joel Sylvester Institute of Cognitive Neuroscience Wellcome Trust Centre for Neuroimging Institute of Neurology University College London ...»

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Richard Joel Sylvester

Institute of Cognitive Neuroscience

Wellcome Trust Centre for Neuroimging

Institute of Neurology

University College London

Prepared under the supervision of:

Professor Geraint Rees

Professor John Driver

Submitted to UCL for the Degree of PhD


I, Richard Sylvester, 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.

Part of the work presented in Chapters 3, 5 and 7 has been published as the following papers.

Sylvester,R., Haynes,J.D., and Rees,G. (2005). Saccades differentially modulate human LGN and V1 responses in the presence and absence of visual stimulation. Current Biology. 15, 37-41.

Sylvester,R., Rees,G. (2006). Extraretinal saccadic signals in human LGN and early retinotopic cortex. Neuroimage. 30(1):214-9.

Sylvester,R., Josephs,O., Driver,J., Rees,G. (2007) Visual FMRI responses in human superior colliculus show a temporal-nasal asymmetry that is absent in lateral geniculate and visual cortex. Journal of Neurophysiology. 97(2):1495-502.


Above all, I would like to thank my supervisor Geraint Rees for his encouragement, guidance, patience and for his invaluable ability to remain positive and enthusiastic in almost any situation. In addition I am very grateful to my second supervisor Jon Driver, whose ability to get to the crux of a problem and then design a workable experiment to test it was crucial in the construction of this thesis.

I would also like to thank the members of the Rees lab – David, Sue, John, Phillip, Bahador, Davina, Rimona, Elaine, Claire, Christian and Ayshe for all their help and advice, and also for the many evenings spent discussing a range of relevant (and trivial) issues in the Queen‟s Larder. In addition without the input of many people at the ICN including Eliot, Stephan, Neil and Christian my time there would have been less productive (and less interesting). Klass and Will were both instrumental in helping with the DCM analysis. Thanks also to all the ICN and FIL support staff – Michelle, Karen, Dominic, Marcia, Amanda, Jan, David, Ric, Rachel, Chris, Lambert and Martin for all their help. Special thanks to Eric, for providing much needed practical support in overcoming a myriad of technical issues.

Thanks also to the Wellcome Trust and the Guarantors of Brain for funding me.

I would also like to thank my family and friends. In particular, Emma, for her unfailing support and many ideas for imaging studies that I did not have time to carry out. Also thanks to Eddie for his willingness to lie in the scanner for many hours oftesting. Thank you to Max, who has been a great distraction during the writing stage of this thesis.

Finally thanks to my parents for making it all possible.

–  –  –

Human motor behaviour depends on the successful integration of vision and eye movements. Many studies have investigated neural correlates of visual processing in humans, but typically with the eyes stationary and fixated centrally. Similarly, many studies have sought to characterise which brain areas are responsible for oculomotor control, but generally in the absence of visual stimulation. The few studies to explicitly study the interaction between visual perception and eye movements suggest strong influences of both static and dynamic eye position on visual processing and modulation of oculomotor structures by properties of visual stimuli. However, the neural mechanisms underlying these interactions are poorly understood.

This thesis uses a range of fMRI methodologies such as retinotopic mapping, multivariate analsyis techniques, dynamic causal modelling and ultra high resolution imaging to examine the interactions between the oculomotor and visual systems in the normal human brain. The results of the experiments presented in this thesis demonstrate that oculomotor behaviour has complex effects on activity in visual areas, while spatial properites of visual stimuli modify activity in oculomotor areas. Specifically, responses in the lateral geniculate nucleus and early cortical visual areas are modulated by saccadic eye movements (a process potentially mediated by the frontal eye fields) and by changes in static eye position. Additionally, responses in oculomotor structures such as the superior colliculus are biased for visual stimuli presented in the temporal rather than nasal hemifield.

These findings reveal that although the visual and oculomotor systems are spatially segregated in the brain, they show a high degree of integration at the neural level. This is consistent with our everyday experience of the visual world where frequent eye movements do not lead to disruption of visual continuity and visual information is seamlessly transformed into motor behaviour.

–  –  –

2.3. fMRI Analysis

2.3.1. Pre-processing Spatial Realignment Coregistration to T1 structural image Spatial Smoothing

2.3.2. Statistical Parametric Mapping Basic approach GLM t and F-statistics

2.4. Retinotopic Mapping

2.4.1. Meridian mapping procedure

2.5. Conclusion……………

–  –  –

5. Chapter 5: Extraretinal saccadic signals in human LGN and early retinotopic cortex

5.1. Introduction

5.2. Methods

5.2.1. Participants

5.2.2. Stimuli and apparatus…

5.2.3. Imaging and analysis

5.2.4. Visual area localisation……………………...

5.3. Results

5.3.1. Eye movement data

5.3.2. FMRI data…………

5.4. Discussion

5.4.1. Saccadic suppression at low stimulus intensity……………... 101 5.4.2. The relationship between extraretinal signals and saccadic suppression………………………………………………….. 101

5.5. Conclusion

–  –  –

7. Chapter 7: Visual responses in human superior colliculus show temporal-nasal asymmetry………………………………

7.1. Introduction

7.2. Methods

7.2.1. Subjects

7.2.2. Stimuli

7.2.3. Imaging and preprocessing

7.2.4. Cortical and subcortical visual area localisation

7.3. Results

7.4. Discussion

7.4.1. FMRI of human superior colliculus

7.4.2. Possible neural substrate for behavioral temporal-hemifield advantages is confirmed in the collicular pathway………….. 149

7.5. Conclusion

8. Chapter 8: General Discussion

8.1. Introduction

8.2. The effects of dynamic oculomotor behaviour on human visual 152 processing……………

8.3. The effects of static eye position on human visual processing.......... 157

8.4. Conclusion

9. References

–  –  –

1.1 Density distribution of cones and rods on the human retina with 15 respect to eccentricity…………………………………………………..

1.2 Cross-section of the human retina at the foveal region demonstrating the foveal pit

1.3 The mapping of the visual field (A) on the LGN (B) and V1 (C) in the macaque monkey

1.4 A letter chart that accurately represents the perceptual consequences of the variation in visual acuity with retinal eccentricity

1.5 The hierarchy of visual areas in the macaque, based on laminar patterns of anatomical connections (including subcortical regions)....... 20

1.6 The dorsal and ventral streams of monkey visual system

1.7 Schematic diagram of the primary structures involved in the neural control of saccades

1.8 The location of V4 neurons presaccadic, perisaccadic and postsaccadic receptive field

2.1 Retinotopic organization of visual areas in the left hemisphere............. 48

2.2 Meridian mapping to identify cortical visual areas in human occipital cortex

2.3 Segmenting white and grey matter in MrGray

2.4 3D rendering of the cortical surface of the right occipital lobe of a single subject

2.5 Unfolded occipital lobe represented as a mesh (left panel) and a flatmap (right panel)

2.6 Functional data from meridian mapping projected onto a flatmap of a single subject‟s left occipital lobe

3.1 Quantification of Ganzfeld conditions

3.2 EOG monitoring of saccadic eye movements during fMRI experiment. 59

3.3 LGN localisation in one representative subject

–  –  –

7.3 Anatomical distribution of physiological noise explained by regressors calculated from the cardiac cycle during EPI volume acquisition…….. 134

7.4 SC responses to contralateral visual field stimulation…………………. 136

7.5 LGN responses to contralateral visual field stimulation………………. 137

7.6 Group average responses (n=8) of human V1-V3, LGN and SC to monocular hemifield visual stimuli presented in the nasal or temporal visual field……………………………………………………………... 139

7.7 Normalised unfitted group average responses (n=8) of V1-V3, LGN and SC to monocular hemifield visual stimuli presented in the nasal or temporal visual field…………………………………………………… 141

7.8 Group average responses (n=8) of V1-V3, LGN and SC to monocular hemifield visual stimuli presented in the nasal or temporal visual field using voxels selected on the basis of response to stimulation via the left OR right eye……………………………………………………….. 142

7.9 Distributions of nasal and temporal field preferences in visually responsive voxels in V1-V3, LGN and SC…………………………….. 144

7.10 Left and right SC voxels plotted according to the degree to which they show eye preference to identical contralateral hemifield stimulation in two representative subjects…………………………………………….. 148

–  –  –


1.1 Introduction Over recent decades there has been remarkable progress towards an understanding of the neural processes that underpin human cognition and behaviour. The prevalent approach, utilised with great success, has involved the study of brain systems (and functions) in relative isolation. While this method has enabled mapping of brain structures according to their predominant function, it has often failed to address how closely related behavioural processes are neurally integrated. The successes and limitations of this method are clearly illustrated by considering the study of human vision and eye movements. The visual system has predominately been investigated by measuring its response to the systematic manipulation of basic visual properties (such as colour, contrast or motion) while other factors affecting visual input such as eye movements are controlled. This method eliminates „confounding‟ effects of eye movements by either presenting visual stimuli very briefly or requiring subjects to maintain central fixation. In contrast, the oculomotor system has largely been investigated by measuring its response to systematic manipulations of oculomotor behaviour in an impoverished visual environment. This approach has resulted in a detailed understanding of the neurophysiology of both the visual and the oculomotor systems, but relatively little information about how they interact.

However, outside of the strictly controlled environment of vision science experiments, successful human behaviour requires that vision and eye movements are highly integrated. For instance, normal vision is characterized by frequent saccades, blinks and changes in the locus of fixation, while oculomotor behaviour usually takes place in a complex and rich visual environment. Some human behavioural studies have indeed demonstrated profound perceptual effects of eye movements on vision (and similarly profound effects of vision on oculomotor behaviour) and in non-human subjects the neural basis of these interactions has been explored. But, the neural mechanisms that subserve successful integration of the visual and oculomotor systems in the human brain are not well defined. This thesis is concerned with investigating these mechanisms to generate an understanding of human vision that reflects the importance of interactions between the visual and oculomotor systems.

1.2 The role of eye movements in human vision In order to appreciate why the visual and oculomotor systems require such close neural integration, one must first consider why eye movements are ubiquitous in human vision.

The most important reason for eye movements is readily apparent from examining the anatomical organisation of the retina and early visual system. The structure of the retina is not homogenous; the fovea is highly specialised for detailed processing of visual information. Although the foveal region represents the central 1º of the visual field, it contains the vast majority of cone photoreceptors that are required for high acuity colour vision (Figure 1.1).

Figure 1.1.

Density distribution of cones and rods on the human retina with respect to eccentricity Cones which carry information about detail and colour are concentrated on the portion of the retina, the fovea, that represents the central portion of the visual field (from Wandell, 1995).

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