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Cognitive Representations in the Sensory and Memory Systems of the Human Brain: Evidence from Brain Damage and MEG

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Cognitive Representations in the Sensory and Memory Systems of the Human Brain: Evidence from Brain Damage and MEG Cognitive Representations in the Sensory and Memory Systems of the Human Brain: Evidence from Brain Damage and MEG Jussi Valtonen Institute of Behavioural Sciences University of Helsinki, Finland Department of Cognitive Science Johns Hopkins University, Baltimore, MD, USA Academic dissertation to be publicly discussed, by due permission of the Faculty of Behavioural Sciences at the University of Helsinki in Auditorium XII of the University Main Building, Unioninkatu 34, on the 16th of May, 2016, at 12 o’clock University of Helsinki Institute of Behavioural Sciences Studies in Psychology 117: 2016 Supervisors Professor Michael McCloskey, PhD, Department of Cognitive Science, Johns Hopkins University, Baltimore, MD, USA Adjunct Professor Hannu Tiitinen, PhD, Department of Engineering and Computational Science, Aalto University, Espoo, Finland Professor Elisabet Service, PhD, Department of Linguistics and Languages, McMaster University, Hamilton, Ontario, Canada Professor Kimmo Alho, PhD, Institute of Behavioural Sciences, University of Helsinki, Finland Reviewers Professor Jane Riddoch, PhD, Department of Experimental Psychology, University of Oxford, Oxford, UK Professor Matti Laine, PhD, Department of Psychology and Logopedics, Åbo Akademi, Turku, Finland Opponent Professor E. Charles Leek, PhD, School of Psychology, Bangor University, Bangor, UK ISSN-L 1798-842X ISSN 1798-842X ISBN 978-951-51-2161-5 (pbk.) ISBN 978-951-51-2162-2 (PDF) http://www.ethesis.helsinki.fi Unigrafia Oy Helsinki 2016 Contents Abstract ..................................................................................................... 5 Tiivistelmä .................................................................................................. 7 Acknowledgments ..................................................................................... 9 List of original publications ...................................................................... 11 Abbreviations ........................................................................................... 12 1. Introduction: Methods in Cognitive Neuroscience ............................... 14 1.1. Methods in cognitive neuroscience and levels of analysis ................................ 15 1.1.1. Experimental studies of patients with cognitive deficits ...................... 16 1.1.2. Electrophysiological methods and functional neuroimaging .............. 19 1.2. Cognitive representations and multiple methods ........................................... 22 2. Part One: Representation of Object Orientation .................................. 23 2.1. Orientation processing in the primate visual system ...................................... 24 2.1.1. Behavioral evidence for orientation processing .................................. 25 2.1.2. Summary .............................................................................................. 30 2.2. Aims of Part One ............................................................................................... 31 2.3. Methods ............................................................................................................. 31 2.3.1. Participants ........................................................................................... 31 2.3.2. Case report ............................................................................................ 31 2.4. Experimental tasks .......................................................................................... 34 2.4.1. Experiment 1: Same-different judgments of arrow orientation ......... 34 2.4.2. Experiment 2: Visual reproduction of line orientation ...................... 36 2.4.3. Experiment 3: Tactile reproduction of line orientation ...................... 41 2.4.4. Experiment 4: Lines with differentiated ends .................................... 44 2.4.5. Discussion ............................................................................................ 48 2.5. Representation of orientation: The COR hypothesis ...................................... 49 2.5.1. The representation of orientation and spatial location ....................... 51 2.5.2. The coordinate-system orientation representation hypothesis ......... 52 2.5.3. Orientation errors and the COR hypothesis ....................................... 56 2.6. General discussion ........................................................................................... 60 3. Part Two: The Neural Basis for the Acquisition of New Memory Representations ................................................................................... 65 3.1. The medial temporal lobe, the hippocampus and human memory ................ 66 3.2. Memory function supported by non-MTL-structures .................................... 68 3.3. Aims of Part Two .............................................................................................. 70 3 3.4. Study III ............................................................................................................ 71 3.4.1. Can non-hippocampal structures support complex learning? ............ 71 3.4.2. Methods ............................................................................................... 74 3.4.3. Results ................................................................................................. 79 3.4.4. Discussion ............................................................................................ 83 3.5. Study IV ............................................................................................................ 85 3.5.1. Does new memory acquisition affect sensory cortical processing? .... 85 3.5.2. Methods ............................................................................................... 92 3.5.3. Results ................................................................................................. 94 3.5.4. Discussion ............................................................................................ 97 3.6. The Neural Basis for the Acquisition of Memory Representations .............. 102 4. General Discussion: Levels of Analysis, Converging Evidence and Methods in Cognitive Neuroscience ................................................... 104 4.1. Levels of analysis and the investigation of cognitive deficits ........................ 104 4.1.1. Advantages of the single-patient method for studies of cognition ... 105 4.1.2. Cognitive theories as a guide for functional neuroimaging .............. 106 4.1.3. Brain-damaged patients and theories of brain function .................... 107 4.1.4. Limitations of the single-patient approach ........................................ 110 4.2. Converging evidence from neuroimaging and studies of brain damage ....... 112 4.3. Levels of analysis and evidence from MEG .................................................... 114 4.3.1. Goals of brain measures and Study IV ............................................... 114 4.3.2. Advantages of MEG ............................................................................ 117 4.4. Further methodological observations ............................................................ 118 4.4.1. Universality, individual variability and cognitive neuroscience ........ 118 4.4.2. Task analysis and cognitive processes .............................................. 120 5. References ......................................................................................... 122 4 Abstract Cognitive representations are constructed internally of events and objects in the outside world. The exact nature of these representations, however, is not fully understood. Studies of cognitive deficits, electromagnetic recordings of brain activity and functional neuroimaging provide complementary means for investigating these representations and their neural basis at multiple levels of analysis. This thesis combined experimental data collected using multiple methods to study cognitive representations and their neural basis in visual information processing and memory. The aim of the thesis was both to collect new empirical evidence to inform current theories of vision and memory, and to use these studies to discuss methodological issues in cognitive neuroscience. The thesis consists of four empirical studies. Studies I-II investigated how spatial information about the orientation of objects is represented in the visual system. Study I was conducted with an individual with a cognitive impairment in visual processing, patient BC. Experimental results from BC showed that spatial orientation is represented compositionally in the visual system, such that the direction of a line orientation’s tilt from a vertical mental reference meridian is coded independently of the magnitude of angular displacement. Further, the cognitive locus of impairment suggested that these representations are maintained at a supra-modal level. Based on experimental evidence from BC and other patients with cognitive deficits in spatial processing, a theoretical framework, the co-ordinate system hypothesis of orientation representation (COR), was proposed in Study II for interpreting orientation errors. Studies III-IV investigated the neural basis for the acquisition of new memory representations in the brain. The medial temporal lobe (MTL) is known to be crucial for declarative memory, but how other brain areas outside the MTL interact to support the construction of new memory representations is not fully understood. Study III investigated new memory acquisition in an amnesic individual, LSJ, who has
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