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The Contribution of the Hippocampus to Language Processing The contribution of the hippocampus to language processing Saleh Alamri ADVERTIMENT. La consulta d’aquesta tesi queda condicionada a l’acceptació de les següents condicions d'ús: La difusió d’aquesta tesi per mitjà del servei TDX (www.tdx.cat) i a través del Dipòsit Digital de la UB (diposit.ub.edu) ha estat autoritzada pels titulars dels drets de propietat intel·lectual únicament per a usos privats emmarcats en activitats d’investigació i docència. No s’autoritza la seva reproducció amb finalitats de lucre ni la seva difusió i posada a disposició des d’un lloc aliè al servei TDX ni al Dipòsit Digital de la UB. No s’autoritza la presentació del seu contingut en una finestra o marc aliè a TDX o al Dipòsit Digital de la UB (framing). Aquesta reserva de drets afecta tant al resum de presentació de la tesi com als seus continguts. En la utilització o cita de parts de la tesi és obligat indicar el nom de la persona autora. ADVERTENCIA. La consulta de esta tesis queda condicionada a la aceptación de las siguientes condiciones de uso: La difusión de esta tesis por medio del servicio TDR (www.tdx.cat) y a través del Repositorio Digital de la UB (diposit.ub.edu) ha sido autorizada por los titulares de los derechos de propiedad intelectual únicamente para usos privados enmarcados en actividades de investigación y docencia. No se autoriza su reproducción con finalidades de lucro ni su difusión y puesta a disposición desde un sitio ajeno al servicio TDR o al Repositorio Digital de la UB. No se autoriza la presentación de su contenido en una ventana o marco ajeno a TDR o al Repositorio Digital de la UB (framing). Esta reserva de derechos afecta tanto al resumen de presentación de la tesis como a sus contenidos. En la utilización o cita de partes de la tesis es obligado indicar el nombre de la persona autora. WARNING. On having consulted this thesis you’re accepting the following use conditions: Spreading this thesis by the TDX (www.tdx.cat) service and by the UB Digital Repository (diposit.ub.edu) has been authorized by the titular of the intellectual property rights only for private uses placed in investigation and teaching activities. Reproduction with lucrative aims is not authorized nor its spreading and availability from a site foreign to the TDX service or to the UB Digital Repository. Introducing its content in a window or frame foreign to the TDX service or to the UB Digital Repository is not authorized (framing). Those rights affect to the presentation summary of the thesis as well as to its contents. In the using or citation of parts of the thesis it’s obliged to indicate the name of the author. The contribution of the hippocampus to language processing Saleh Alamri A thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy to the Doctoral Program in Cognitive Science and Language, Section of General Linguistics, Universidad de Barcelona Supervisor Professor Cedric Boeckx ICREA Universitat de Barcelona June 2017 Acknowledgement First and foremost I would like to thank my PhD advisor, Professor Cedric Boeckx, for his invaluable support and advice during these past four years, and for being so encouraging in the pursuit of new ideas. The work in this thesis could not have been accomplished without his generous help. I appre- ciate all his contributions of time, ideas, funding and the many wonderful opportunities he gave me during my PhD. The joy and enthusiasm he has for his research was contagious and motivational for me. My time at the Universitat de Barcelona was made enjoyable in large part due to my group members, our discussions and comments were immensely fruitful. I am very grateful for the BIB group members, Constantina The- ofanopoulou, and Thomas ORourke. I give special thanks to Pedro Tiago Martins for his technical support. Similarly, profound gratitude goes to the ministry of education in Saudi Ara- bia for providing the funding that allowed me to undertake this research. Then, there are many friends to thank, including my partner in crime, Guil- laume Thuilliez. It is a pleasure to thank all my friends for the wonderful times we shared. Special mention goes to Marta Nadal for her love and patience, her encour- agement during the final stages of my research is so appreciated. Finally, my deep and sincere gratitude goes to my family for their help and support during my studies. I am forever indebted to my parents for giving me the opportunities and experiences that have made me who I am. i Abstract Humans display distinct unlimited capacity to produce expressions in lan- guage and use them flexibly in language processing.This characteristic of human language allows speakers to use novel, flexible, and complex struc- tures during communication. Neurobiologically, however, it is not fully un- derstood how the rapid process of language production and language com- prehension occurs, including word generation, interpretations and common representations that facilitate the process of real-time language processing. The classical theories and approaches have limited the language network to perisylvian cortical regions, namely the Broca's and Wernicke's areas. This thesis proposes that the language network goes beyond the cortical regions indicated by traditional views. In doing so, this thesis puts forward a hy- pothesis that subcortical structures are not only fundamental to memory but also to language, in which online language processing receives a ma- jor contribution from the hippocampal declarative memory, which allows speakers and listeners to use language flexibly. The mechanism of such a contribution by the hippocampal declarative memory system during online language processing is via relational binding in which hippocampal declar- ative memory rapidly retrieves a network of relative, stored information to serve in the particular context. To support the hypothesis of hippocampal implications in language pro- cessing, several pathologies that affect the hippocampus have been reviewed, including Alzheimer's disease, Down syndrome, Williams' syndrome, schizophre- nia, depression and bipolar disorder. The review evaluated hippocampal neurobiological alterations in each pathology, and determined cognitive and language profiles. Findings from previous pathologies indicate that the hip- pocampus affects language at two levels. First, in the general delay in lan- guage acquisition and other cognitive aspects, and second, in the disturbed use of language during online communication; short lag interaction is seen to occur when the hippocampal formation is lesioned. It appears that hip- pocampal lesions suppress the flexible use of stored information within cer- tain contexts in communication, as it does in flexible navigation in animal models. This thesis concludes that the hippocampus is a multi-cognitive operator that is implicated in several cognitive areas including the flexible use of language during real-time processing, and therefore it should be taken into account in the language network in the human brain. ii Contents 1 Introduction 1 1.1 Classical neuropsychology of language . .2 1.2 Pathways for language . .3 1.3 Anatomy of the hippocampal formation . .9 1.4 The hippocampus and cognitive flexibility in animals . 16 1.5 Aims and hypotheses . 20 2 Hippocampal function in cognition 22 2.1 Hippocampus and language . 22 2.1.1 Relational binding . 29 2.1.2 Neural binding . 36 2.1.3 Verbal communication . 43 2.1.4 Default mode network . 49 2.1.5 Dopamine and the hippocampus . 50 3 Alzheimer's disease 56 3.1 Brian morphology and Alzheimer's disease . 56 3.2 Cognitive profile in AD . 62 3.3 Language profile in AD . 65 i 3.4 Discussion . 68 4 Down Syndrome 71 4.1 Brain morphology in Down syndrome . 72 4.2 DYRK1A . 76 4.3 RCAN1 . 78 4.4 Cognitive profile in DS . 79 4.5 Language profile in DS . 81 4.5.1 Oral motor development . 81 4.5.2 Semantics . 83 4.5.3 Syntax . 84 4.6 Discussion . 86 5 Williams' Syndrome 90 5.1 Introduction . 90 5.2 Brain morphology in Williams' syndrome . 91 5.2.1 LIMK1 . 95 5.2.2 CYLN2 . 97 5.2.3 FZD9 . 98 5.3 Cognitive profile in WS . 99 5.4 Language profile in WS . 103 5.5 WS and 7q11.23 duplication syndrome . 105 5.6 Discussion . 107 6 Schizophrenia, Depression and Bipolar Disorder 109 6.1 Introduction . 109 6.2 Structural brain alterations in SZ . 110 6.3 Cognitive profile in schizophrenia . 115 ii 6.4 Language profile in schizophrenia . 117 6.5 Depression and bipolar disorder . 119 6.6 Cognitive profile in MD and bipolar disorder . 121 6.7 Language profile in MD and bipolar disorder . 123 6.8 Discussion . 126 7 Concluding remarks and future directions 128 iii List of Tables 1.1 A: Continuum between close-ended and open-ended song learn- ing. Adapted from(Brenowitz and Beecher, 2005). B: Hip- pocampal volume (the volumes are in cubic millimetres and have been log transformed), (Devoogd et al., 1993). 16 4.1 Brain alteration in various brain structures in Down syn- drome throughout life. Adapted from (Dierssen, 2012). 74 5.1 Comparable measurement of hippocampal volumes between WS and healthy individuals. Adapted from (Meyer-Lindenberg et al., 2005b). 93 iv List of Figures 1.1 Brain image of Broca's and Wernicke's areas in the left hemi- sphere of the human brain. .3 1.2 Illustration of arcuate fasciulus connecting frontal and parietal- temporal cortex in the left hemispheres of human brain, in- cluding Broca's area and Wernicke's area. Adapted from (Catani and De Schotten, 2008). .4 1.3 Humans evolved a solid form of arcuate fasciulus compared to chimpanzees and macaque monkeys (Ghazanfar, 2008).
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