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Plasticity in the Human Hippocampus Plasticity in the Human Hippocampus Katherine Woollett Submitted for PhD in Cognitive Neuroscience October 2010 University College London Supervisor: Eleanor A. Maguire Declaration: I, Katherine Woollett, 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: Abstract If we are to approach rehabilitation of memory-impaired patients in a systematic and efficacious way, then it is vital to know if the human memory system has the propensity for plasticity in adulthood, the limiting factors on such plasticity, and the timescales of any plastic change. This thesis was motivated by an attempt to develop a body of knowledge in relation to these questions. There is wide agreement that the hippocampus plays a key role in navigation and memory across species. Evidence from animal studies suggests that spatial memory- related hippocampal volume changes and experience-related hippocampal neurogenesis takes place throughout the lifespan. Previous studies in humans indicated that expert navigators, licensed London taxi drivers, have different patterns of hippocampal grey matter volume relative to control participants. In addition, preliminary evidence also suggested there may be functional consequences associated with this grey matter pattern. Using licensed London taxi drivers as a model for learning and memory, the work undertaken centered on four key issues: (1) In a set of studies, I characterised the neuropsychological profile of licensed London taxi drivers in detail, which included devising a number of new table-top associational memory tests. This enabled me to assess the functional consequences of their expertise and hippocampal grey matter pattern in greater depth than previous studies. (2) In order to explore the effects of taxi drivers’ expertise in more naturalistic settings, I also examined how well they could learn the layout of an unfamiliar town compared with a group of non-taxi drivers, and how effectively taxi drivers could integrate a new district into their existing spatial representation of London. (3) I then conducted a study on experts whose knowledge was much less spatial than taxi drivers in order to examine if the effects on hippocampal grey matter and neuropsychology were general or whether they were specific to the spatial domain. (4) Given that previous taxi driver studies were cross-sectional, the question of whether the human hippocampus can exhibit spatial memory-related structural plasticity in adulthood was uncertain. I therefore conducted a longitudinal study which assessed participants both pre and post taxi driver training using structural MRI and neuropsychological measures. This enabled me to investigate, within subjects, whether hippocampal volume changes can be acquired in response to intense spatial stimulation. In addition, I explored whether ceasing to be a taxi driver (i.e. retiring after many years on the job) resulted in ‘reverse’ plasticity. I found evidence for hippocampal plasticity within individuals as a result of their intense acquisition of spatial knowledge over a number of years that was associated with qualifying to be a licensed London taxi driver, and preliminary evidence of reverse plasticity when taxi drivers retire. This suggests that hippocampal structure and memory ability can be modified in response to environmental factors and are not necessarily hard-wired. However, my results also provide some insights into the boundaries within which human memory operates, as I identified both positive and negative cognitive consequences of being an expert navigator, and also established that the MRI and neuropsychology effects of expertise on the hippocampus may be restricted to the spatial domain. Acknowledgements The work in this thesis could not have been accomplished without the generous help of a number of people. I wish to thank Prof. Eleanor Maguire, my principal supervisor, for her invaluable support and advice throughout my PhD, and for being so encouraging, enthusiastic and patient, and Prof. Neil Burgess, my secondary supervisor. Next there are my friends and colleagues to thank from UCL: Nikolaus Weiskopf, Chloe Hutton and John Ashburner for their technical advice; Alex Leff and Jenny Crinion for being so helpful and generous with their time; Alice Neal, Debbie Talmi and Jen Summerfield for making me smile; the support staff at the FIL; Peter Aston, David Bradbury, Janice Glensman, Ric Davis and Chris Freemantle for help with scanning and computers. Finally, I would like to thank my mother, Beto and Marga Martin for teaching me to never give up, without which I would not have been here today doing this PhD. Table of Contents Chapter 1- Does experience change the brain? 12 1.1 Introduction 13 1.2 Structural effects of expertise in the healthy adult human brain 17 1.3 Hippocampal anatomy 19 1.4 The functions of the hippocampus 26 1.5 Structural changes in the hippocampus 31 1.6 Licensed London taxi drivers – a model system 33 1.7 What are the underlying mechanisms of plasticity? 42 1.8 Functional differentiation along the long-axis of the hippocampus 49 1.9 Thesis overview 54 Chapter 2 - Materials and Methods 56 2.1 Introduction 57 2.2 Participants 57 2.3 Biophysics of magnetic resonance imaging 60 2.3.1 Magnetic fields 60 2.4 Generating an MR signal 62 2.5 Tomographic image formation 64 2.6 Scanning parameters 64 2.7 Structural MRI sequences 66 2.8 Automated analysis of structural MRI scans 69 2.8.1 Standard voxel-based morphometry (VBM) 69 2.8.2 Diffeomorphic Anatomical Registration using Exponentiated Lie algebra (DARTEL) 71 2.8.3 High Dimensional Warping 71 2.9 Statistical inference 72 2.10 Neuropsychological tests 73 Chapter 3 - The effects of navigational expertise: an in-depth analysis 75 3.1 Introduction 76 3.2 Experiment 1 78 3.2.1 Materials and methods 78 3.2.2 Procedure 89 3.2.3 Data analysis 89 3.3 Results 90 3.3.1 MRI data 90 i 3.3.2 Neuropsychological data 91 3.4 Discussion 97 3.5 Experiment 2 101 3.5.1 Material and Methods 102 3.5.2 Procedure and data analyses 107 3.5.3 Results 107 3.5.4 Discussion 108 Chapter 4 -The effects of navigational expertise on wayfinding in new environments 111 4.1 Introduction 112 4.2 Experiment 3 114 4.2.1 Materials and methods 114 4.2.2 Procedure 123 4.2.3 Data analysis 123 4.2.4 Results 124 4.2.5 Discussion 132 Chapter 5 - Non-spatial expertise and hippocampal grey matter volume 139 5.1 Introduction 140 5.2 Experiment 4 142 5.2.1 Material and methods 142 5.2.2 Procedure 144 5.2.3 Data analyses 144 5.2.4 Results 144 5.2.5 Discussion 148 Chapter 6 - Hippocampal plasticity: a longitudinal study 151 6.1 Introduction 153 6.2 Experiment 5 158 6.2.1 Materials and methods 158 6.2.2 Procedure 162 6.2.3 Data analyses 162 6.2.4 Results: Time 1 163 6.2.5 Results: Time 2 167 6.2.6 Results: Time 1 vs. Time 2 171 6.2.7 Discussion 174 6.3 Experiment 6 177 6.3.1 Material and methods 178 6.3.2 Procedure 182 ii 6.3.3 Data analysis 183 6.3.4 Results 183 6.3.5 Discussion 186 Chapter 7 - General discussion 188 7.1 Plasticity in the human hippocampus 190 7.2 Neuropsychological consequences of navigational expertise 196 7.3 Spatial and non-spatial expertise 201 7.4 Implications for the hippocampus 203 7.5 Conclusions 205 References 208 iii List of Figures Figure 1. Example of a sagittal view from a structural MRI scan 14 Figure 2. The human hippocampal formation 19 Figure 3. Schematic representation of the hippocampal network 20 Figure 4. Hippocampal place cells 24 Figure 5. Navigation performance 29 Figure 6. Map of London 34 Figure 7. Taxi driver qualification process 35 Figure 8. Hippocampal volume differences between taxi drivers and control subjects 37 Figure 9. The effect of taxi driving experience on grey matter volume 39 Figure 10. Main effects for the neuropsychological tests 40 Figure 11. Newly generated cells can be detected in the adult human hippocampus in patients 48 Figure 12. 3D modelling of molecularly defined subdivisions of DG, CA3, and CA1 delineated by gene expression 52 Figure 13. Protons align parallel or anti-parallel to the magnetic field (B0) 62 Figure 14. Generation of MR signal 63 Figure 15. T1 weighted scan - Structural MRI image showing different tissue intensities 66 Figure 16. The Rey-Osterrieth complex figure 84 Figure 17. Example of London landmark recognition test stimuli 86 Figure 18. Example of London proximity judgements test stimuli 87 Figure 19. Object–place associations test 89 Figure 20. Anterior hippocampal grey matter volume differences between taxi drivers and control subjects 92 Figure 21. London proximity judgements 94 Figure 22. Object-place test 96 Figure 23. Visual paired associates test 104 Figure 24. Visual paired associates within a scene context test 104 Figure 25. Face-name associations test 105 Figure 26. Object-sound associations test 106 Figure 27. Verbal paired associates 107 Figure 28. Map of New Town 116 Figure 29. Map of London 120 Figure 30. Example views from the three environments 121 Figure 31. Example sketch maps 126 Figure 32. Scenes correctly recognised across environments 129 Figure 33. Road segments recalled across environments 130 Figure 32. Road junction recalled across environments 131 Figure 35. Knowledge in medical doctors 147 Figure 36. Grey matter differences between qualified London taxi drivers 173 Figure 37. The virtual environment of London (UK) 182 iv Figure 38. MRI findings in retired taxi drivers 185 Figure 39. Rey complex figure 186 Figure 40.
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