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Neural Circuit Mechanisms of Stimulus Selection Underlying Spatial Attention

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Neural Circuit Mechanisms of Stimulus Selection Underlying Spatial Attention NEURAL CIRCUIT MECHANISMS OF STIMULUS SELECTION UNDERLYING SPATIAL ATTENTION by Nagaraj R. Mahajan A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland February 2020 © 2020 Nagaraj R. Mahajan All Rights Reserved Abstract Humans and animals routinely encounter competing pieces of information in their environments, and must continually select the most salient in order to survive and behave adaptively. Here, using computational modeling, extracellular neural recordings, and focal, reversible silencing of neurons in the midbrain of barn owls, we uncovered how two essential computations underlying competitive selection are implemented in the brain: a) the ability to select the most salient stimulus among all pairs of stimulus locations, and b) the ability to signal the most salient stimulus categorically. We first discovered that a key inhibitory nucleus in the midbrain attention network, called isthmi pars magnocellularis (Imc), encodes visual space with receptive fields that have multiple excitatory hotspots (‘‘lobes’’). Such (previously unknown) multilobed encoding of visual space is necessitated for selection at all location-pairs in the face of scarcity of Imc neurons. Although distributed seemingly randomly, the RF lobe-locations are optimized across the high-firing Imc neurons, allowing them to combinatorially solve selection across space. This combinatorially optimized inhibition strategy minimizes metabolic and wiring costs. ii Next, we discovered that a ‘donut-like’ inhibitory mechanism in which each competing option suppresses all options except itself is highly effective at generating categorical responses. It surpasses motifs of feedback inhibition, recurrent excitation, and divisive normalization used commonly in decision-making models. We demonstrated experimentally not only that this mechanism operates in the midbrain spatial selection network in barn owls, but also that it is required for categorical signaling by it. Moreover, the pattern of inhibition in the midbrain forms an exquisitely structured ‘multi-holed’ donut consistent with this network’s combinatorial inhibitory function (computation 1). Our work demonstrates that the vertebrate midbrain uses seemingly carefully optimized structural and functional strategies to solve challenging computational problems underlying stimulus selection and spatial attention at all location pairs. The neural motifs discovered here represent circuit-based solutions that are generalizable to other brain areas, other forms of behavior (such as decision-making, action selection) as well as for the design of artificial systems (such as robotics, self-driving cars) that rely on the selection of one among many options. Thesis committee Advisor and First Reader: Dr. Shreesh P. Mysore Second Reader: Dr. Hynek Hermansky Committee members: Dr. Mounya Elhilali, Dr. Ralph Etienne-Cummings iii Acknowledgments My PhD thesis would not have been possible if not for the support, both professionally and personally from many people in my life. I am very grateful to my advisor Dr. Shreesh P. Mysore for his immense support and mentorship through the course of my PhD, and for providing me a home in his lab. I had the fortune of meeting Shreesh through Dr. Hynek in my first year. He was kind enough to offer me a rotation in his lab despite my lack of experience in neuroscience. I had a great time during the rotation as he was always available for discussions, and was willing to spend hours together on meetings to answer even basic neuroscience questions. This cemented my decision to join his lab over the other labs I was considering at that point. Over the years, the excitement and passion with which he spoke about research has been extremely contagious. I have learnt so much through our uncountable meetings and discussions that many times lasted for several hours. Through these discussions, he not only shared his knowledge about the field of neuroscience, but also imparted his wisdom about his experiences going through various phases of an academic and research career. I am thankful for the training he provided me with for performing experiments and surgeries. Rather than relying on some preexisting data to model with, this gave me the iv freedom to design and perform experiments to answer questions that were of direct relevance to our dynamically evolving research findings. For this reason, I am glad that I pursued a combination of experimental and computational neuroscience for my PhD. As we worked through figuring out the computational principles associated with some of our exciting (at least to us) experimental findings, I learnt from him how to frame a fundamentally important research question and answer it methodically. Working on both the ‘combinatorial inhibition’ and ‘categorization’ projects has been such an exciting, fulfilling and enjoyable experience for me. From Shreesh, I have also learnt the value of writing and presenting results in a compelling manner. Additionally, he gave me extremely valuable feedback on numerous research presentations across the years, and my ability to present a talk has significantly improved over the years, thanks to his feedback and time. When I joined Shreesh’s lab, I was quite surprised at his willingness to accept me, someone with no experimental background, into his lab and to train me in doing some really challenging neuroscience experiments. Looking back after all these years though, I realize that it was just a mere reflection of who Shreesh is as a person, and of his scientific and mentorship principles. As I ventured into a totally new field, there were obviously numerous times where I doubted myself. But his endless encouragement and patience helped me instill a strong belief in my decision to explore the magical world of neuroscience, something I have come to love so dearly. I will be eternally grateful that he was willing to take a chance on me and invest in me, for I have benefitted and learnt a lot from it. As I culminate my thesis, I do feel that I have not only found a mentor and an advisor, but also a friend in Shreesh to whom I can reach out to, as I continue pursuing research in the coming years of my life. v I also have a lot to thank to Hynek for. When I told him in my first year that I was interested in neuroscience, he was extremely supportive and encouraged me to follow what I was truly interested in, even though I had come to Hopkins with an intention of working with him for my PhD. He not only gave me a neuroscience project to explore the area to see if it matched my interests, but also met numerous neuroscience professors along with me to see if we could work on potential collaborative projects. I am grateful for his mentorship and advice across the years related not just to science, but also career. I enjoyed working with him on projects related to STRF analyses. I thank him for his guidance and advice, both in that project and my thesis work. I thank Dr. Mounya Elhilali and Dr. Ralph Etienne-Cummings for serving on my thesis committee; Dr. James Knierim, Dr. Noah Cowan and Dr. Cynthia Moss for serving on my gradual board oral committee; and Dr. Sanjeev Khudanpur and Dr. Trac Tran for serving on my department qualifying exam committee. Their comments and feedback at various points of my PhD were extremely valuable in putting together this thesis. I reached out to Dr. Rene Vidal and Dr. Amitabh Basu to discuss some aspects of my research, and getting their perspective was very helpful in thinking about the broader impact of my project. I also thank Dr. Hita Adwanikar for giving feedback about my projects during lab research presentations. I thank Dr. James Knierim for his valuable and patient feedback on our papers. My interest in pursuing a PhD and research in general is credited to the wonderful set of professors I had the fortune of working with during my bachelor’s degree at IIT Hyderabad. My undergraduate thesis advisor, Dr. Sri Rama Murty’s ability to dissect a complicated problem and solve it with a systematic approach is something I will only hope to achieve one day. Dr. Soumya Jana encouraged me to not be overwhelmed by difficult problems. As I vi struggled through the open-ended research problem he gave us as course projects, the meetings and conversations with him taught me to break down big problems into smaller solvable ones, and to celebrate any progress as a victory. My interest in neuroscience and the biomedical field broadly began due to my work with Dr. Sumohana Channappayya on using image processing techniques for analyzing retinal scan images. That project made me realize that I could use my background in DSP in interdisciplinary fields, and evidently, that has had a lasting impact on me as I culminate this thesis in neuroscience. The experience I gained by working with the three of them during my formative years will stay with me for the rest of my life. I also fondly remember the courses by Dr. Balasubramaniam Jayaram. I hope that if I end up becoming a teacher one day, I could teach like him. Staying far away from family in a different country would have been infinitely harder if not for the support system from lab mates and friends at Hopkins. Over the years, I have learnt so much from my brilliant, extremely smart and kind lab mates: Wen-Kai, Margo, Juliana, Hannah, Ninad, Garima and Barbara. It has been absolutely great to share my PhD journey with you guys and learn from your journeys and projects. I have had numerous discussions with all of them about my research work, especially with Ninad, Wen-kai and Margo. Coffee and lunch conversations became a regular occurrence once Ninad joined the lab. I have discussed my research with him quite extensively, and getting his thoughts on it always made me think harder about my work.
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