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Sensorimotor Transformation and Information Coding Across Cortex During Perceptual Decisions

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Sensorimotor Transformation and Information Coding Across Cortex During Perceptual Decisions Sensorimotor transformation and information coding across cortex during perceptual decisions by Gerald N. Pho B. S. E., Biomedical Engineering Case Western Reserve University, 2010 SUBMITTED TO THE DEPARTMENT OF BRAIN AND COGNITIVE SCIENCES IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN NEUROSCIENCE AT THE MASSACHUSETTS INSTITUTE OF TECHNOLOGY JUNE 2017 © Massachusetts Institute of Technology. All rights reserved. Signature of Author………………………………......………………………………………….. Department of Brain and Cognitive Sciences April 12, 2017 Certified by……………………….……………………………………………………………….. Mriganka Sur Paul E. Newton Professor of Neuroscience Thesis Supervisor Accepted by……………………………………………………...……………………………….. Matthew A. Wilson Sherman Fairchild Professor of Neuroscience and Picower Scholar Director of Graduate Education for Brain and Cognitive Sciences 1 2 Sensorimotor transformation and information coding across cortex during perceptual decisions by Gerald N. Pho Submitted to the Department of Brain and Cognitive Sciences on April 12, in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Neuroscience ABSTRACT Perceptual decision-making is an important and experimentally tractable paradigm for uncovering general principles of neural information processing and cognitive function. While the process of mapping sensory stimuli onto motor actions may appear to be simple, its neural underpinnings are poorly understood. The goal of this thesis is to better understand the neural mechanisms underlying perceptual decision-making by exploring three major questions: How is decision- relevant information encoded across the cortex? What cortical areas are necessary for perceptual decision-making? And finally, what neural mechanisms underlie the mapping of sensory percepts to appropriate motor outputs? We investigated the roles of visual (V1), posterior parietal (PPC), and frontal motor (fMC) cortices of mice during a memory-guided visual decision task. Large-scale calcium imaging revealed that neurons in each area were heterogeneous and spanned all task epochs (stimulus, delay, response). However, information encoding was distinct across regions, with V1 encoding stimulus, fMC encoding choice, and PPC multiplexing the two variables. Optogenetic inhibition during behavior showed that all regions were necessary during the stimulus epoch, but only fMC was required during the delay and response epochs. Stimulus information was therefore rapidly transformed into behavioral choice, requiring V1, PPC, and fMC during the transformation period, but only fMC for maintaining the choice in memory prior to execution. We further investigated whether the role of PPC was specific to visual processing or to sensorimotor transformation. Using calcium imaging during both engaged behavior and passive viewing, we found that unlike V1 neurons, most PPC neurons responded exclusively during task performance, although a minority exhibited contrast-dependent visual responses. By re-training mice on a reversed task contingency, we discovered that neurons in PPC but not V1 reflected the new sensorimotor contingency. Population analyses additionally revealed that task-specific information was represented in a dynamic code in PPC but not in V1. The strong task dependence, heterogeneity, and dynamic coding of PPC activity point to a central role in sensorimotor transformation. By measuring and manipulating activity across multiple cortical regions, we have gained insight into how the cortex processes information during sensorimotor decisions, paving the way for future mechanistic studies using the mouse system. Thesis Supervisor: Mriganka Sur Title: Paul E. Newton Professor of Neuroscience 3 4 Acknowledgements It takes a community to make a Ph.D., and mine is no exception. There are many people who made this thesis possible and who made my experience in grad school an unforgettable time of learning and personal transformation. First, I am very indebted to my thesis advisor, Mriganka Sur, who has been a wonderful mentor and support for me over these years. His contagious enthusiasm, sharp intellect, and persistent encouragement were all essential to my completion of this thesis and my development as a scientist. If given the opportunity to lead a lab, I hope that I can emulate both his inspirational passion for science as well as his unconditional generosity as a mentor. I would also like to thank the other members of my thesis committee: Bob Desimone, Chris Harvey, and Matt Wilson. Each of them played important roles over the years in providing critical feedback, helping me to write fellowships, and giving career advice. The members of the Sur laboratory, past and present, have provided a wonderful environment to learn and do science over the years. I am fortunate to have had an amazing collaborator and mentor in Michael Goard, a former postdoc in the lab, who played a critical role not only in this thesis but also in my development as a scientist. Almost every aspect of this thesis was a team effort between the two of us, and I am grateful to have had the opportunity to work closely with someone as talented and generous as Mike. Rafiq Huda was another important collaborator and friend with whom I had countless scientific discussions that were very fruitful for my growth. And there are many others in the lab who I had the privilege of working with and learning from: Jacque Ip, Rajeev Rikhye, Ming Hu, Travis Emery, Vincent Breton-Provencher Sami El-Boustani, Vardhan Dani, Liadan Gunter, Benjamin Crawford, and Jonathan Woodson. I am especially grateful for friends like Jacque and Rajeev. We tried to “get fit” together, but much more often we just “got fat” together instead – but in the end what counts is that we got friends. Speaking of friends, there are many, many others who not only made these years far more enjoyable for me, but who also inspired and encouraged me through all the ups and downs. The MIT Graduate Christian Fellowship was truly my family during my time here. Being part of this community not only enriched my experience of graduate school, but it also helped me to learn how to give every area of my life to Christ. I must especially thank Thomas, Sam P, Ming and Yukkee, Peng and Annie, and Sam E for inspiring me, walking with me, challenging me, and praying for me over the years. I am lucky also to have been part of the Sidney-Pacific small group for the past three years. I would especially thank Frank, Megan, Hosea, Linyi, Yunming, and AJ for being such a consistent support and source of encouragement and prayer. There are many other friends who made these years so wonderful, whether from MIT, Park Street Church or from my undergrad (Boston CWRU!): Gideon, Janet, Karen, Ben, Ruthie, Jared, Binna, Jessica, Alex, James, and Ted. There are four friends to whom I owe a special debt of gratitude. I met three of them in my first year of grad school, and I now consider each of them closer than brothers. I am grateful for such a reliable friend in David who was a consistent voice of truth and sanity over the years. Mark, John and I have been praying together weekly for nearly six full years. While I cannot hope to describe the full impact they have had on me, I must thank them for challenging me to live out my convictions, and for lifting me up when I did not have strength to do so. And the final friend I must thank is Stephanie. Though our friendship has only blossomed relatively recently, I am tremendously grateful for the one who so patiently and persistently affirmed me over the past year and a half, and who has given me a new joy that I am hopeful will persist for years to come. 5 I am very proud to dedicate this thesis to my family. It has been wonderful to see my relationship with my sister JoAnn grow only deeper even as we have grown further apart in distance. I am so thankful for her encouragement and support. But most of all, I would like to thank my parents. As immigrants and refugees from Vietnam after the war, they worked tirelessly and from scratch to give me the opportunities I have today. As Chinese parents who prize discipline, integrity, and hard work, they taught me to value education and encouraged me to seek the highest possible degree I could receive. Though I can never repay them for their sacrifices for me, I am proud to represent them as the first Ph.D. in our family, and to dedicate this body of work to their unceasing love. Last and foremost, I would like to thank and praise God, who has been my strength, my hope, and my joy over the past years and beyond. He has been faithful through all the ups and downs of my grad school years, even when I have been faithless. Looking back I stand amazed at all He has done to transform me from a self-oriented and insecure person into one with a deeper capacity to love others and pursue his beauty and truth. May this thesis be just one more testimony of all that He can and will do by the power of His love. 6 Table of Contents Chapter 1: Introduction ............................................................................................... 10 1.1 Background .......................................................................................................... 10 1.2 Overall organization of thesis ............................................................................... 18 1.3 References ........................................................................................................... 20 Chapter 2: Neural signatures of a
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