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Episodic Memory and the Hippocampus

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The Neural Processes Underpinning Episodic Memory Demis Hassabis Submitted for PhD in Cognitive Neuroscience February 2009 University College London Supervisor: Eleanor A. Maguire 1 Declaration: I, Demis Hassabis, 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: 2 Abstract Episodic memory is the memory for our personal past experiences. Although numerous functional magnetic resonance imaging (fMRI) studies investigating its neural basis have revealed a consistent and distributed network of associated brain regions, surprisingly little is known about the contributions individual brain areas make to the recollective experience. In this thesis I address this fundamental issue by employing a range of different experimental techniques including neuropsychological testing, virtual reality environments, whole brain and high spatial resolution fMRI, and multivariate pattern analysis. Episodic memory recall is widely agreed to be a reconstructive process, one that is known to be critically reliant on the hippocampus. I therefore hypothesised that the same neural machinery responsible for reconstruction might also support ‘constructive’ cognitive functions such as imagination. To test this proposal, patients with focal damage to the hippocampus bilaterally were asked to imagine new experiences and were found to be impaired relative to matched control participants. Moreover, driving this deficit was a lack of spatial coherence in their imagined experiences, pointing to a role for the hippocampus in binding together the disparate elements of a scene. A subsequent fMRI study involving healthy participants compared the recall of real memories with the construction of imaginary memories. This revealed a fronto-temporo- parietal network in common to both tasks that included the hippocampus, ventromedial prefrontal, retrosplenial and parietal cortices. Based on these results I advanced the notion that this network might support the process of ‘scene construction’, defined as the generation and maintenance of a complex and coherent spatial context. Furthermore, I argued that this scene construction network might underpin other important cognitive functions besides episodic memory and imagination, such as navigation and thinking about the future. It is has been proposed that spatial context may act as the scaffold around which episodic memories are built. Given the hippocampus appears to play a critical role in imagination by supporting the creation of a rich coherent spatial scene, I sought to explore the nature of this hippocampal spatial code in a novel way. By combining high 3 spatial resolution fMRI with multivariate pattern analysis techniques it proved possible to accurately determine where a subject was located in a virtual reality environment based solely on the pattern of activity across hippocampal voxels. For this to have been possible, the hippocampal population code must be large and non-uniform. I then extended these techniques to the domain of episodic memory by showing that individual memories could be accurately decoded from the pattern of activity across hippocampal voxels, thus identifying individual memory traces. I consider these findings together with other recent advances in the episodic memory field, and present a new perspective on the role of the hippocampus in episodic recollection. I discuss how this new (and preliminary) framework compares with current prevailing theories of hippocampal function, and suggest how it might account for some previously contradictory data. 4 To Alexander and Arthur The best in me ‘It's a poor sort of memory that only works backwards’ (Lewis Carroll, the White Queen to Alice in “Through the Looking-Glass”) 5 Acknowledgements The work in this thesis could not have been accomplished without the generous help of a number of people. I wish to thank Eleanor Maguire, my principal supervisor, for her invaluable support and advice throughout my PhD, and for being so encouraging of new ideas. I want to also thank Geraint Rees, my second supervisor, for his guidance and infectious enthusiasm. Then there are my friends and colleagues to thank from UCL: my partner in crime Dharshan Kumaran; Dean Mobbs for opening the door to exciting collaborations; Hugo Spiers and Benedetto de Martino for interesting science discussions; Carlton Chu and Martin Chadwick for work on multivariate methods; Jennifer Summerfield and Katherine Woollett for help on scene construction; Neil Burgess and Caswell Barry for useful theoretical discussions; Nikolaus Weiskopf and John Ashburner for their technical advice; and the support staff at the FIL, particularly Peter Aston, David Bradbury, Janice Glensman and Ric Davis for help with scanning and computers. Thanks also to the Brain Research Trust and the Wellcome Trust for funding the work in this thesis. Finally, I would like to thank my mother and father for their spiritual and intellectual encouragement during my formative years without which I would not have been here today doing this PhD. And of course, most importantly, thanks to Teresa Niccoli who puts up with my craziness somehow and without whose love and support none of this could have happened. 6 Contents 1. Episodic Memory and the Hippocampus................................................................15 1.1 Introduction............................................................................................................16 1.2 Episodic memory...................................................................................................18 1.3 Reconstructive theories of episodic memory recall ...............................................21 1.4 The brain network underpinning episodic memory................................................23 1.4.1 The hippocampus ......................................................................................................... 23 1.4.2 The episodic memory network...................................................................................... 27 1.5 Hippocampal population codes .............................................................................29 1.5.1 Information in the brain................................................................................................. 30 1.5.2 The cell assembly hypothesis....................................................................................... 31 1.5.3 Invariant representations in the hippocampus.............................................................. 33 1.5.4 Properties of the hippocampal population code ........................................................... 34 1.5.4.1 Sparse codes......................................................................................................... 34 1.5.4.2 Topographical organisation ................................................................................... 35 1.6 Thesis overview............................................................................................................... 36 2. Theories of Hippocampal Function.........................................................................39 2.1 Introduction............................................................................................................40 2.2 The Marr model .....................................................................................................41 2.3 Declarative theory..................................................................................................42 2.4 Multiple trace theory ..............................................................................................46 2.5 Cognitive map theory.............................................................................................50 2.6 Relational theory....................................................................................................55 2.7 Summary ...............................................................................................................60 3. Methods .....................................................................................................................62 3.1 Introduction............................................................................................................63 3.2 The biophysics of magnetic resonance imaging (MRI)..........................................63 3.2.1 Magnetic fields.............................................................................................................. 63 3.2.2 Generating an MR signal.............................................................................................. 65 3.2.3 Tomographic image formation...................................................................................... 67 3.2.4 Scanning parameters ................................................................................................... 67 3.3 The BOLD signal ...................................................................................................69 3.3.1 The BOLD effect........................................................................................................... 69 7 3.3.2 The neurophysiology of the BOLD signal..................................................................... 70 3.4 Resolution of fMRI.................................................................................................72 3.5 Analysis of fMRI data.............................................................................................73
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