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How the Layout of Primary Visual Cortex (V1) Shapes Higher Cognitive Functioning

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When size matters: how the layout of primary visual cortex (V1) shapes higher cognitive functioning Johanna Bergmann A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy I UNSW At! ST ·~ALl A School of Psychology Faculty of Science January, 2015 Originality Statement Originality Statement ‘I hereby declare that this submission is my own work and to the best of my knowl- edge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgement is made in the thesis. Any contribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project’s design and conception or in style, presentation and linguistic expression is acknowledged.’ Johanna Bergmann January, 2015 5 6 Acknowledgments Acknowledgments ”Commuting” around the globe between the UNSW in Sydney and the Max Planck Institute for Brain Research in Frankfurt on a regular basis has both been an exciting and exhausting experience. I’ve learned so many things during my PhD and there are many people who I would like to thank. First, I would like to thank Joel Pearson at UNSW, for your dedicated supervision and support, which made doing my PhD in two far-distant places very smooth and easy. I truly appreciate your openness and courage to think outside the box. Second, Wolf Singer at the MPI, for letting me pursue my projects in your department, which offers such an inspiring and motivating environment to do research. Your knowledge is amazing, and whenever I was at a loss, I knew I could always rely on your wise and helpful input. Third, my coworkers Erhan Genç and Axel Kohler, for your great support in my projects. It has been a pleasure to work with people who are so kind and warm-hearted and at the same time so skillful and knowledgeable. I’ve very much enjoyed working with you and hope there will be opportunity to do so again in the future. Fourth, Ulrich Pilatus, who joined in for the third project, for your fantastic support and technical advice. Last but not least, I would like to thank the department secretaries at the MPI, Ulrike Radden and Michaela Wicke, for your great assistance in all organizational issues, and the IT and Technical support units at both the MPI and at UNSW for your generous and reliable support. Of course, many people apart from the world of science contributed to help me maintain the right mindset to keep doing what I needed to do. First of all, I would like to thank my parents, who are always there for me and support me in any way they can. My sister, who makes me consider things from a different angle. My awesome friends in Germany that I can always count on, most importantly Isabella, Mareike, Heidi, Sophie, Simon, Steffi and Roman. The new friends I’ve made during my time here in Sydney and our amazing weekends full of surfing, rock climbing, white-water rafting and kayaking, canyoning and all the other fun things that helped me keep perspec- tive. All this was such a perfect counterbalance to science and has made my time here in Sydney so special. Sarah and Simon for hosting me in the first few weeks after my arrival in Sydney, and Annika and Benni for making me feel at home in Bondi. Sar- ah, Stefan, Alexandra, Wen Jun and the rest of the “gang” for the craziness. Then, of course, I would like to thank my great office and lab mates, in particular Nina Merkel, Will Barnes and Andreas Sauer at the MPI and the girls on level 15 at UNSW, most importantly Briana Kennedy, Alice Towler and Diana Matovic. It was so much more fun to come in every day with you around. Last, but not least, I would like to thank 7 Tobias Weis. I still can’t believe my luck to have stumbled into you in Sydney. You’re the best thing that could have ever happened to me – thank you so much for joining me in this journey for the past two years and for making everything just so much more awesome. 8 Notes related to this thesis Notes related to this thesis The study in Chapter 2 has been published: Bergmann, J., Genç, E., Kohler, A., Singer, W., & Pearson, J. (2014). Neural anatomy of primary visual cortex limits visual working memory. Cerebral Cortex, doi:10.1093/cercor/bhu168. An edited version of the study in Chapter 3 has been submitted: Bergmann, J., Genç, E., Kohler, A., Singer, W., & Pearson, J. (submitted). Smaller primary visual cortex is associated with stronger, but less precise mental imagery. Data of the study in Chapter 4 will be submitted in: Bergmann, J., Pilatus, U., Genç, E., Kohler, A., Singer, W., & Pearson, J. (to be submitted). V1 surface size predicts GABA concentration in medial occipital cortex. Bergmann, J., Pilatus, U., Genç, E., Kohler, A., Singer, W., & Pearson, J. (to be submitted). Individual differences in fMRI resting-state activity are predicted by rest- ing glutamate concentration. 9 10 Thesis Abstract Thesis Abstract Human beings are endowed with a wide range of highly developed cognitive abil- ities. Which factors have led to this level of intellectual capacity in the course of evo- lution? In cross species studies, overall brain size is a reliable predictor of cognitive perfor- mance, but more specific information about how the brain’s structural and functional organization may be linked to these enhancements is lacking. The aim of this thesis was to investigate the role of the anatomy and function of the primary visual cortex (V1) in behaviour. V1 is the earliest sensory stage for vision in the cerebral cortex, and is responsible for processing low-level visual features such as spatial orientation, loca- tion and frequency. Interestingly, V1 size displays huge variance between individuals; this offers an amazing opportunity to study the behavioural effect of brain enlarge- ment within a human sample while avoiding the various confounds that can distort the results in cross species studies. Previous research has shown that a larger V1 is linked to higher perceptual sensitiv- ity; but to what extent these size differences may also affect higher cognitive functions is unknown. Using a combined approach of behavioural testing and fMRI brain imag- ing methods, we find that the acuity of two cognitive functions, namely the precision of visual imagery and visual working memory storage, are significantly positively cor- related with the surface size of V1: individuals with a larger V1 tended to have more precise imagery and greater visual working memory storage. In contrast, the strength of visual imagery was negatively related to V1 surface size. In addition, we find that other indices of neural function, such as the concentra- tion of the inhibitory neurotransmitter GABA in the medial occipital cortex and V1 spontaneous functional activity levels, covaried significantly with differences in V1 surface size. Our findings support the notion of a positive relationship between brain (areal) size and cognition and show how even very low-level sensory areas are involved in shaping our intellect. As a last point, we discuss the potential limitations of the posi- tive link between brain size and cognitive ability. 11 12 Content Overview 01 General Introduction 19 02 Neural anatomy of primary visual cortex limits 51 visual working memory 03 Smaller primary visual cortex is associated with 83 stronger, but less precise mental imagery 04 Individual V1 size and its relationship to occipital 123 GABA levels and V1 fMRI resting-state activity 05 General Discussion 159 13 Content Originality Statement ....................................................................................................................5 Acknowledgments ..........................................................................................................................7 Notes related to this thesis .........................................................................................................9 Thesis Abstract ............................................................................................................................. 11 Overview ....................................................................................................................................... 13 01 General Introduction 19 1.1 Evolution of the brain ..........................................................................................................21 1.1.1 The radial unit hypothesis .........................................................................................21 1.1.2 What happens when the brain gets bigger?...........................................................24 1.2 Primary visual cortex (V1) architecture .........................................................................26 1.2.1The topography of VI ...................................................................................................26 1.2.2 Characteristic properties of V1 neurons ...............................................................28 1.2.3 Implications of individual differences in V1 size ....................................................30 1.3 Higher cognitive functioning and the brain .....................................................................34 1.3.1 Concepts and properties of visual working memory .........................................35
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