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Three-Dimensional Space Representation in the Human Brain

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Three-Dimensional Space Representation in the Human Brain 1 Three-dimensional space representation in the human brain Misun Kim Submitted for a PhD in Cognitive Neuroscience May 2018 Supervisor: Eleanor A. Maguire 2 I, Misun Kim, 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. Signed: _________________________ Date: __________________________ 3 Abstract Brain structures that support spatial cognition by encoding one’s position and direction have been extensively studied for decades. In the majority of studies, neural substrates have been investigated on a horizontal two-dimensional plane, whereas humans and other animals also move vertically in a three-dimensional (3D) world. In this thesis, I investigated how 3D spatial information is represented in the human brain using functional MRI experiments and custom-built 3D virtual environments. In the first experiment, participants moved on flat, tilted-up or tilted-down pathways in a 3D lattice structure. Multivoxel pattern analysis revealed that the anterior hippocampus expressed 3D location information that was similarly sensitive to the vertical and horizontal axes. The retrosplenial cortex and posterior hippocampus represented direction information that was only sensitive to the vertical axis. In the second experiment, participants moved in a virtual building with multiple levels and rooms. Using an fMRI repetition suppression analysis, I observed a hierarchical representation of this 3D space, with anterior hippocampus representing local information within a room, while retrosplenial cortex, parahippocampal cortex and posterior hippocampus represented room information within the wider building. As in the first experiment, vertical and horizontal location information was similarly encoded. In the last experiments, participants were placed into a virtual zero-gravity environment where they could move freely along all 3 axes. The thalamus and subiculum expressed horizontal heading information, whereas retrosplenial cortex showed dominant encoding of vertical heading. Using novel fMRI analyses, I also found preliminary evidence of a 3D grid code in the entorhinal cortex. Overall, these experiments demonstrate the capacity of the human brain to implement a flexible and efficient representation of 3D space. The work in this thesis will, I hope, 4 serve as a stepping-stone in our understanding of how we navigate in the real – 3D – world. 5 Impact statement Our world is three-dimensional (3D). We navigate in multi-level buildings, on undulating terrain and in the open air. However, the neural circuitry underlying spatial cognition (our “internal GPS system”) has mainly been studied on horizontal two-dimensional (2D) surfaces. The experiments I report here extend our understanding of spatial cognition by incorporating the uncharted third dimension. I used custom-built virtual reality navigation paradigms and a non-invasive brain scanning technique (functional magnetic resonance imaging - fMRI) to test where, and how, 3D location and direction information is encoded in the human brain. The main findings were: (1) the hippocampus contained information about where participants were in 3D environments and it was similarly sensitive to vertical and horizontal axes; (2) 3D heading was collectively encoded by the thalamus, subiculum and retrosplenial cortex, and these brain areas were sensitive to either horizontal or vertical direction; (3) the brain seemed to have flexible representations of 3D space, adapted for the shape of environments and behavioural demands. My work will hopefully promote further research into 3D spatial cognition in both humans and other animals, as we still know so little about this crucial aspect of cognition. For example, the retrosplenial cortex, which represented vertical direction information in my fMRI studies, is a candidate brain structure to contain head direction cells tuned to vertical pitch, and this could be tested in animal electrophysiological studies. Taking the lead from my work, which revealed the basic neural circuitry for 3D spatial representations, future research should seek to elucidate how we actively navigate and find goals in a realistic 3D world. This might help us to develop better navigation strategies. I also showed the advantage of using virtual reality techniques and a quasi-naturalistic setup, and I believe similar approaches should be deployed more widely in the field of spatial research. 6 The impact of my research also extends beyond the domain of spatial navigation. Recent findings suggest that the brain uses a map-like code to solve more general cognitive problems, such as social interactions, perception and decision making. The analysis methods I developed – including probing 3D grid codes using fMRI – could be applied to broader cognitive problems which are inherently high-dimensional. In the longer term, studying 3D spatial representation might bring clinical benefits. The hippocampus, entorhinal cortex and retrosplenial cortex – the main brain structures investigated in my work – are early casualties in Alzheimer’s disease, and spatial disorientation is a common initial symptom. The prognostic value of 2D grid signals in the brain has been previously suggested, but spatial navigation tasks in 3D might be more sensitive in aiding early detection of impending cognitive decline. It may sound far-fetched, but understanding the neural basis of our sense of direction in 3D could be pertinent when humans are freed from Earth’s gravity. Space exploration is an ever-increasing endeavour (e.g. missions to Mars by NASA and commercial companies). An understanding of 3D space representations in the brain will be crucial to facilitating the ergonomic design of microgravity environments during space travel. 7 Acknowledgements I first want to give my enormous thanks to my primary supervisor, Eleanor Maguire. She was extremely generous with her time, teaching me how to do science, how to write, how to talk and, most importantly, how to keep my chin up when science occasionally tested me. I have always been supported and trusted by her, and this is by far the best thing any supervisor can do. I will miss our regular Tuesday meetings. I am grateful to my funders, the Wellcome Trust (“for the incurably curious”) and Samsung Scholarship. I also want to thank my ~120 participants who bore my experiments without VR sickness or claustrophobia (my apologies to the few people who were afflicted). I was so lucky to get my PhD training at the Wellcome Centre for Human Neuroimaging (aka the “FIL”). All of the staff (Kamlyn, Peter, David, IT, the radiographers, etc.) provided awesome support. The scientific advice was excellent (Karl, the guru, who patiently reminded me of Neyman Pearson lemma, Guillaume who helped me to excavate SPM, Pete Z, Gareth, Martina, Tim Behrens). I can’t imagine my PhD without the Maguire gang – Anna, Conny, Daniel, Dina, Gloria, Ian, Marshall + honorary member Swan – who have always lifted me up scientifically and in many other ways. Thanks to my amazing office mates who rescued me from my 2D desk space to the outside 3D world like Nitzan, Thomas, Philipp, Claudia, Mona, Sofie, Alexa, Pradeep, Michael, etc. I also want to say thanks to Alasdair Gibb and David Attwell – the Wellcome 4 year PhD committee – who brought me to UCL and kindly looked after me in my first year and onwards. Special thanks to Fabio and Elina in my PhD program. Thanks also to my secondary supervisor, Kate Jeffery, who sowed the seed of 3D space research. Last, but not least, I am eternally grateful to my beloved family in Korea. 항상 믿어주고 기도해주는 엄마, 아빠, 형주, 민서야 고마워. 8 Table of contents Abstract ........................................................................................................................ 3 Impact statement .......................................................................................................... 5 Acknowledgements ....................................................................................................... 7 Table of contents .......................................................................................................... 8 List of figures .............................................................................................................. 11 List of tables ............................................................................................................... 14 List of abbreviations .................................................................................................... 15 Chapter 1 General introduction .............................................................................. 16 1.1 Overview ....................................................................................................... 16 1.2 Place cells in 3D space ................................................................................. 18 1.3 Head direction cells in 3D space ................................................................... 23 1.4 Grid cells in 3D space ................................................................................... 29 1.5 Boundary cells and other spatial cells in 3D space ........................................ 35 1.6 Behavioural studies in 3D space ................................................................... 38 1.7 Human neuropsychological, neuroimaging and electrophysiological studies in 3D space .................................................................................................................
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