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ATTENTION AND AWARENESS: VISUAL PSYCHOPHYSICS AND AVERSIVE CONDITIONING IN HUMANS Thesis by Naotsugu Tsuchiya In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy California Institute of Technology Pasadena, California 2006 (Defended July 18, 2005) ii 2006 Naotsugu Tsuchiya All Rights Reserved iii Acknowledgement As I write this acknowledgement, I remember all the exciting events and troubles that happened to me one after another since I came to Caltech. I started as a volunteer researcher in April 2000 and joined the CNS program as a graduate student during that summer. Over these five years, I’ve been fortunate to be surrounded by my colleagues and friends, whom I want to acknowledge here. Mark Konishi and Shin Shimojo have been my role models of successful Japanese researchers in the American academic community. I owe a lot to their advice and encouragement throughout my graduate life at Caltech. Especially, Shin’s recommendation to Christof Koch in April 2000 made it possible for me to work as a volunteer. My Caltech life started from there. I introduced myself in a five-minute meeting to Christof, trying to convince him that I was desperately interested in the problem of consciousness and that I wanted to work in his lab. It was the most intense five minutes. He took the risk of taking me. I only hope I have brought more fruit than troubles to him. I cannot imagine such a great (and colorful) advisor like him if I were in Japan. Jochen Braun was the advisor for my first project on visual motion and attention (Chapter 3). I thank him for his generous invitation to England and Germany, which makes me think that I should be generous to him even if our manuscript will never be published. Working with Geraint Rees at University College London on this motion and attention project with functional magnetic resonance imaging (fMRI) was very exciting. Through this project, I learned a lot about visual psychophysics and fMRI. iv McKell Carter taught me how to conduct electrical shock experiments with Caltech students (and sometimes with our mentor!) in the name of science. Throughout the collaboration with him, we published one paper and submitted another one now in the second round of the review (in Chapter 4), at the cost of a few friends who really hated the electrical shocks. I thank more than 200 subjects who participated in our ‘uncomfortable but not painful’ experiments (See Method 4.4.1). Ryota Kanai at the Universiteit Utrecht, the Netherlands, has been my best friend, colleague, and rival since we shared our office in Kyoto University, Japan, in 1999-2000. With Ryota, I translated Christof’s “The Quest for Consciousness” into Japanese as a private project. We will continue our collaboration. I thank all of my colleagues in the Koch lab, past and present. Connie Hofstoetter and Farshad Moradi were very helpful with my project on afterimage using continuous flash suppression. I enjoyed the collaboration with Melissa Saenz as well as two of my SURF students, Bobby Rohrkemper and Dania Adamuszek. Kamran Diba invited me to give a talk at Rutgers, The State University of New Jersey, which was a very good experience for me. I organized several parties in the Koch lab, which went very well usually. I was pleased when people liked the sushi, which Dirk Walther and I prepared at the farewell party for the Reddy sisters. There is one thing I do regret, however: it was my mistake to introduce karaoke to Patrick Wilken and Wei Ji Ma at the farewell party for Chunhui Mo. I am grateful to my committee for two candidacy exams and the defense: Yaser Abu-Mostafa, Pietro Perona, David Dubowitz, Joe Bogen, Ralph Adolphs, John O’Doherty, Steve Quartz, Richard Andersen. v My wife, Noriko, has supported and encouraged my research throughout. She has been keeping an eye on my health, both mental and physical. Nori’s comments on my practice talks before conferences have been always critical and useful. We shared one joy when I received the Best Student Presentation Award in the ASSC 9 conference in June of 2005. Nori and I often let out our stress at parties with our Japanese friends. These Japanese friends were my secret pool for many of my psychophysics experiments. Finally, I want to thank my family, Hisao, Junko, and Rie for their generous support and encouragement. vi Abstract We studied the neuronal correlates of consciousness by characterizing the role of attention and awareness in three psychophysical experiments. First, we investigated the role of visual awareness in the formation of afterimages, phenomena believed to occur in the retina. Visibility of the afterimage-inducing stimuli was manipulated by a powerful dichoptic suppression technique, continuous flash suppression, which allows us to project visual stimuli onto the retina without subjects noticing them at all, sometimes longer than three minutes. We found that reliably suppressing the inducer weakens afterimage strength. Paradoxically, trial-to-trial variability in visibility did not correlate with the intensity of afterimage. As afterimages are enhanced when attention is withdrawn from the adaptor, the opposite effects between awareness and attention were demonstrated. Second, we examined visual motion processing outside the focus of spatial, top-down attention using a dual-task paradigm. Attentional effects in motion processing were characterized by our novel wavelet motion stimuli. Our stimuli effectively activate neurons in the first stage of motion processing, while they are poor stimuli for higher motion processing. Using a contrast-masking paradigm, we found that attention mainly affected the strength of inhibition for high-contrast motion stimuli in an orientation- specific, but not direction-specific manner, presumably reflecting the physiological properties for divisive inhibition within the primary visual cortex. Third, we characterized the role of awareness in classical aversive conditioning. Subjects associated previously neutral auditory stimuli (CS) with aversive mild electric shocks (US). We used skin conductance response, an index for autonomic arousal, as implicit measure for vii the conditioned response. In delay conditioning, CS was paired with delayed but overlapping US, while in trace conditioning CS was followed by US after a three-second temporal gap. We intermixed these two CSs with another control CS that never predicted US to examine whether awareness plays different roles depending on the temporal relationships between CS and US. Subjects expressed their shock expectancy using their gaze direction, from which we inferred the onset of awareness of CS-US contingency. By aligning the skin conductance response with the onset of awareness, we found that trace, but not delay, conditioning coincided with the onset of awareness. viii Table of contents ACKNOWLEDGEMENT ...............................................................................................................III ABSTRACT ....................................................................................................................................... VI TABLE OF CONTENTS..............................................................................................................VIII LIST OF FIGURES.........................................................................................................................XII LIST OF TABLES .........................................................................................................................XIII LIST OF ABBREVIATIONS ...................................................................................................... XIV CHAPTER 1........................................................................................................................................ XIV CHAPTER 2........................................................................................................................................ XIV CHAPTER 3........................................................................................................................................ XIV CHAPTER 4........................................................................................................................................ XIV 1. GENERAL INTRODUCTION..................................................................................................1 1.1. THE NEURONAL CORRELATES OF CONSCIOUSNESS.............................................................. 1 1.2. OUR THREE APPROACHES TO THE SEARCH FOR THE NCC ................................................. 3 1.3. STRUCTURE OF THE THESIS ..................................................................................................... 8 2. ROLE OF AWARENESS AND ATTENTION IN THE FORMATION OF NEGATIVE AFTERIMAGES..................................................................................................................................9 2.1. OVERVIEW ................................................................................................................................. 9 2.2. SUMMARY................................................................................................................................. 12 2.3. INTRODUCTION........................................................................................................................ 13 2.4. CHARACTERIZING CONTINUOUS FLASH SUPPRESSION (CFS) ......................................... 16 2.4.1. EXPERIMENT 1: PROLONGED INVISIBILITY BY CFS...........................................................
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