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Genetic Dissection of Circuits Underlying the Modular Structure of the Superior Colliculus

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Genetic Dissection of Circuits Underlying the Modular Structure of the Superior Colliculus Genetic dissection of circuits underlying the modular structure of the Superior Colliculus Laura Masullo MRC Laboratory of Molecular Biology University of Cambridge This dissertation is submitted for the degree of Doctor of Philosophy Peterhouse March 2019 Declaration This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except as declared in the Statement of Contribution. All the work described in this dissertation was carried out in the Neurobiology Division of the Medical Research Council Laboratory of Molecular Biology, under the supervision of Dr. Marco Tripodi. It is not substantially the same as any that I have submitted, or, is being concurrently submitted for a degree or diploma or other qualification at the University of Cambridge or any other University or similar institution. I further state that no substantial part of my dissertation has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution. It does not exceed 60,000 words, excluding figures, tables, appendices and bibliography, as specified by the Degree Committee. I II Statement of contributions Due to the interdisciplinary nature of this project, some of the data presented was acquired and analysed with the help of the following collaborators: Dr. Letizia Mariotti (Tripodi Lab): acquired and analysed part of the electrophysiological recordings in vitro (Chapter 3), contributed to the implementation of the double-sensor system for head movement tracking (Chapter 5), assisted with the analysis of optogenetics data (Chapter 6) and conducted the in vivo electrophysiology experiments (Chapter 7). Nicolas Alexandre (Tripodi Lab): contributed to the implementation of the double-sensor system for head movement tracking (Chapter 5). Dr. Paula Freire-Pritchett (LMB Bioinformatics Unit): developed the software for the analysis of RNAseq datasets (Chapter 3). Jerome Boulanger (LMB Light Microscopy Unit): developed the software for the analysis of 3D images acquired with light sheet microscopy (Chapter 3). All experiments in this thesis were conceived and designed by my PhD supervisor, Dr. Marco Tripodi, and myself, with additional input from other investigators for the experiments they contributed to. III IV Summary In order to successfully interact with the environment, animals need to produce accurate movements towards specific positions in space. A crucial region of the brain that guides such goal-oriented movements is the superior colliculus (SC), an evolutionary conserved structure of the midbrain. While several lines of research in different model organisms have confirmed that the SC contributes to the initiation of orienting movements, how functionally distinct neuronal groups within the SC are organized to support the production of such motor outputs is poorly understood. One of the reasons why the intrinsic circuit organization of the SC remains elusive is the lack of genetic characterization of the neuronal populations of the motor SC. Here, we performed RNAseq to screen for genetic markers for neuronal subpopulations in the motor SC. We identified a transcription factor, Pitx2, which is exclusively expressed in a subpopulation of glutamatergic neurons in the motor domain of the SC. Strikingly, this population of neurons displays a non-homogenous distribution within the motor layer of the SC, being organised in clusters along the mediolateral and anteroposterior axis. We mapped the pre-synaptic network and the post-synaptic targets of Pitx2ON neurons, unveiling that this modular population receives direct inputs from motor and sensory cortical regions, as well as several midbrain nuclei involved in movement control, and sends projection along the cephalomotor pathway. We then asked whether these modules may act as functional units, each integrating multimodal sensory information and encoding a specific feature of head movement, the main ethologically relevant orienting behaviour in rodents. Optogenetic activation of this modular population in freely moving animals produced a stereotyped, robust head motion characterised by a pronounced quantal nature; furthermore, the amplitude of the elicited head movement varied based on the modular unit activated. Our results suggest that distinct clusters of genetically defined neurons produce head displacement along a characteristic vector. In conclusion, we found that a population of premotor neurons in the SC is organised in a modular conformation and we suggest that such modularity may represent a physical implementation of a discontinuous motor map for orienting movements encoded in the mouse SC. Our work complements previous observations of periodicity in SC circuitry, as well as its afferent and efferent systems. Exploiting the genetic toolkit available in the mouse, our work begins to address the functional relevance of this modularity and paves the way for future experiments to investigate principles of sensorimotor integration in SC circuits. V VI Acknowledgements I would like to thank my supervisor Marco Tripodi for giving me the opportunity to join the lab, entrusting me with this exciting project and supervising me through its realisation. I would also like to thank the following people: Letizia Mariotti, a great collaborator, brilliant scientist and exceptional friend; I will forever be grateful for her unconditional help and constant support during my PhD. I could not have asked for a better companion to embark on this demanding project. Members of the Tripodi Lab, for scientific discussions, coffee breaks and moral support. Michael Hastings, for his advice throughout my graduate studies. Claire Knox and the Biological Services group, for their invalueable technical assistance. Steve Scotcher and the LMB Mechanical Workshop, for finding a way to accommodate all my last minute requests. Peterhouse, and in particular my MCR committee, for providing a home away from home. My parents and Giulio, for always offering the source of greatest comfort and unrivalled encouragement. VII VIII Table of contents Declaration I Statement of contributions III Summary V Acknowledgements VII List of abbreviations XV 1. INTRODUCTION ....................................................................................... 1 1.1 The neuroscience of space ................................................................................................................ 1 1.1.1 Navigating in space .................................................................................................................. 2 1.1.2 Interacting with space .............................................................................................................. 3 1.2 Orienting actions: translating the world into motor space ................................................................ 4 1.2.1 Goal-oriented actions ............................................................................................................... 5 1.2.2 Sensing a non-visual space ....................................................................................................... 7 1.3 The superior colliculus: a unique spatial hub ................................................................................... 9 1.3.1 Eye movements ....................................................................................................................... 10 1.3.2 Head movements ..................................................................................................................... 11 1.3.3 Tactile orienting ..................................................................................................................... 12 1.3.4 Auditory and sonar localization ............................................................................................. 13 1.3.5 Spatial attention in the SC ...................................................................................................... 14 1.4 Anatomical substrates for sensorimotor integration in the SC ....................................................... 15 1.4.1 Lamination defines functional domains .................................................................................. 15 1.4.2 Inputs to the SC ...................................................................................................................... 19 1.4.3 Anatomical outputs of the SC…………………………………………………………………………19 1.4.4 Intracollicular circuits for sensorimotor processing………………………………………...……20 1.5 Genetic approach to neural circuits ................................................................................................ 22 1.5.1 A universal definition of cell types.......................................................................................... 22 1.5.2 Genetics of neural circuits ...................................................................................................... 23 1.5.3 Genetic tools in murine system ............................................................................................... 23 1.6 Aims of the study ........................................................................................................................... 26 2. METHODS ................................................................................................. 29 2.1 Animal strains ...............................................................................................................................
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