CENTER FOR SYSTEMS ENGINEERING AND APPLIED MECHANICS AND LABORATORY OF NEUROPHYSIOLOGY The use of extraretinal information to compensate for self-movement GUNNAR BLOHM Thesis submitted in partial fulfillment of the requirements for the degree of Docteur en Sciences Appliquées Jury: Prof. Vincent Blondel (FSA, UCL) Prof. J. Douglas Crawford (Center for Vision Research, York University, Toronto) Prof. Marc Crommelinck (MD, UCL) Prof. Philippe Lefèvre (FSA, UCL, promoter) Prof. Guillaume Masson (Centre de Recherche en Sciences Cognitives, CNRS, Marseille) Prof. Marcus Missal (MD, UCL) ACKNOWLEDGEMENTS The work that I accomplished during the last few years and that resulted in the thesis text you hold in your hands right now would not have been possible without the contribution of many people. I would like to express my gratitude to all the members of the Centre for Systems Engineering and Applied Mechanics as well as the Laboratory of Neurophysiology for the friendly working ambiance. My deepest considerations go to Prof. Philippe Lefèvre. He was for me a mentor, friend and example. I am also very thankful to Prof. Marcus Missal for his fresh ideas, his friendly consideration and all the fun we had together. And the kindness and support of Prof. Marc Crommelinck was always an invaluable motivation for me. I am also indebted to Prof. Vincent Blondel for accepting to preside over the thesis jury. My special thanks go the external members of the thesis jury. Prof. Guillaume Masson and Prof. J. Douglas Crawford kindly accepted to critically examine the preliminary version of the manuscript. Their comments, questions and suggestions largely enhanced its quality. I will not forget all the present and former members of the oculomotor research group. My special thanks go to my former officemate Sophie de Brouwer for her precious help with the experimental set-up. Although constantly in a hurry, Demet Yüksel was always present to provide medical (she is a clinical ophthalmologist) and mental support. Aside all the fun we had together, I also obtained great assistance from Jean-Jacques Orban de Xivry to conduct the experiments that used the Cambridge Visual Stimulus Generator. Thank you and all the others for your friendship. Finally, I would like to express my deepest gratitude to my family and particularly to my wife Annick, who supported me with courageous patience and loving kindness. And the smile and joy of my son Joachim was a permanent source of decompression and happiness. To my lovely wife Annick and to my son Joachim, our little sunshine. TABLE OF CONTENTS CHAPTER I........................................................................................ 1 INTRODUCTION – SCIENTIFIC BACKGROUND .................... 1 1. THE SCOPE OF THIS WORK.......................................................... 1 2. THE EYE AND ITS MOVEMENTS .................................................. 2 2.1. The eye plant, extra-ocular muscles and brainstem signals ........................................................................................... 2 2.2. Saccades ............................................................................. 4 2.2.1. General behavior...................................................... 4 2.2.2. Latencies .................................................................. 5 2.2.3. Model ....................................................................... 7 2.2.4. Neurophysiology...................................................... 7 2.3. Smooth pursuit.................................................................... 9 2.3.1. General behavior...................................................... 9 2.3.2. Model ....................................................................... 9 2.3.3. Neurophysiology.................................................... 10 2.4. Other eye movements........................................................ 11 3. INTERACTION BETWEEN SMOOTH PURSUIT AND SACCADES ..... 12 3.1. Velocity input to the saccadic system............................... 12 3.2. Position input to the smooth pursuit system..................... 15 3.3. Common neural pathways................................................ 16 4. EXTRARETINAL SIGNALS AND THE SENSE OF MOTION.............. 18 4.1. The role of proprioception in oculomotor control ........... 18 4.2. Efferent feedback loops and eye movements .................... 20 4.3. Self-generated motion and space constancy .................... 22 4.3.1. Eye position information........................................ 22 TABLE OF CONTENTS 4.3.2. Tracking self-generated motion............................. 23 4.3.3. Open questions and motivation of this thesis ........ 24 5. CONTENT OF THE THESIS ......................................................... 26 6. LIST OF PUBLICATIONS ............................................................ 28 6.1. Journal articles : .............................................................. 28 6.2. Journal articles submitted:............................................... 28 6.3. Conference abstracts:....................................................... 28 CHAPTER II .................................................................................... 31 PROCESSING OF RETINAL AND EXTRARETINAL SIGNALS FOR MEMORY GUIDED SACCADES DURING SMOOTH PURSUIT .......................................................................................... 31 1. ABSTRACT............................................................................... 31 2. INTRODUCTION........................................................................ 32 3. EXPERIMENTAL PROCEDURES.................................................. 34 3.1. Experimental set-up.......................................................... 34 3.2. Paradigm.......................................................................... 35 3.3. Data acquisition and analysis .......................................... 37 4. RESULTS.................................................................................. 39 4.1. Programming of 1st saccade............................................. 41 4.2. Saccadic latency distribution ........................................... 48 4.3. Time course of orientation ............................................... 58 5. DISCUSSION............................................................................. 60 5.1. Saccadic reaction times.................................................... 61 5.2. Saccades compensate for self-motion............................... 62 5.3. Hypothesized underlying neural mechanisms .................. 65 CHAPTER III................................................................................... 69 INTERACTION BETWEEN SMOOTH ANTICIPATION AND SACCADES DURING OCULAR ORIENTATION IN DARKNESS ...................................................................................... 69 1. ABSTRACT............................................................................... 69 2. INTRODUCTION........................................................................ 70 3. MATERIALS AND METHODS..................................................... 72 3.1. Experimental set-up.......................................................... 72 3.2. Paradigm.......................................................................... 72 3.3. Data acquisition and analysis .......................................... 74 4. RESULTS.................................................................................. 75 TABLE OF CONTENTS 4.1. General saccadic properties ............................................ 77 4.2. Programming of the first saccade .................................... 80 4.3. Time course of orientation ............................................... 84 5. DISCUSSION............................................................................. 90 5.1. Saccade properties ........................................................... 91 5.2. Programming of the first orienting saccade..................... 91 5.3. Time course of the orientation process ............................ 92 5.4. Proposed model................................................................ 93 6. CONCLUSION ........................................................................... 96 CHAPTER IV................................................................................... 97 SMOOTH ANTICIPATORY EYE MOVEMENTS ALTER THE MEMORIZED POSITION OF FLASHED TARGETS............... 97 1. ABSTRACT............................................................................... 97 2. INTRODUCTION........................................................................ 98 3. METHODS ................................................................................ 99 3.1. Experiment 1..................................................................... 99 3.1.1. Experimental set-up............................................... 99 3.1.2. Paradigm .............................................................. 100 3.1.3. Data acquisition and analysis............................... 101 3.2. Experiment 2................................................................... 102 3.2.1. Experimental set-up............................................. 102 3.2.2. Paradigm .............................................................. 103 3.2.3. Data acquisition and analysis............................... 103 4. RESULTS................................................................................ 104 4.1. Experiment 1................................................................... 104