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Understanding the Building Blocks of Avian Complex Cognition : The Understanding the building blocks of avian complex cognition: the executive caudal nidopallium and the neuronal energy budget by Kaya von Eugen A thesis submitted in partial fulfilment of the requirements for the degree of Philosophiae Doctoris (PhD) in Neuroscience From the International Graduate School of Neuroscience Ruhr University Bochum September 30th 2020 This research was conducted at the Department of Biopsychology, within the Faculty of Psychology at the Ruhr University under the supervision of Prof. Dr. Dr. h.c. Onur Güntürkün Printed with the permission of the International Graduate School of Neuroscience, Ruhr University Bochum Statement I certify herewith that the dissertation included here was completed and written independently by me and without outside assistance. References to the work and theories of others have been cited and acknowledged completely and correctly. The “Guidelines for Good Scientific Practice” according to § 9, Sec. 3 of the PhD regulations of the International Graduate School of Neuroscience were adhered to. This work has never been submitted in this, or a similar form, at this or any other domestic or foreign institution of higher learning as a dissertation. The abovementioned statement was made as a solemn declaration. I conscientiously believe and state it to be true and declare that it is of the same legal significance and value as if it were made under oath. Bochum, 30.09.2020 Kaya von Eugen PhD Commission Chair: PD Dr. Dirk Jancke 1st Internal Examiner: Prof. Dr. Dr. h.c. Onur Güntürkün 2nd Internal Examiner: Prof. Dr. Carsten Theiß External Examiner: Prof. Dr. Andrew Iwaniuk Non-Specialist: Prof. Dr. Patrik Krieger Date of Final Examination: 9th of December 2020 PhD Grade Assigned: magna cum laude If a bird may think, its thoughts are not so small, For it may think of skies or hills or anything at all. So a child may think, thoughts big and free and wide— It's good for birds and children, thoughts need not fit inside. ~Annette Wynne Table of Contents List of Figures ........................................................................................................ I List of Tables ........................................................................................................ III List of Abbreviations ........................................................................................... V Abstract ............................................................................................................... IX Chapter 1 General introduction ...................................................................... 1 1.1 Introduction ................................................................................................... 3 1.2 Phylogeny of mammals, reptiles and birds .................................................... 5 1.2.1 The last common ancestor of amniotes .................................................. 5 1.2.2 Synapsids and mammals ........................................................................ 6 1.2.3 Sauropsids and reptiles .......................................................................... 7 1.3 Behaviour and cognition of mammals, reptiles and birds ............................... 8 1.3.1 Cognition and complex cognition in birds, reptiles and mammals ........... 9 1.4 Brains of mammals, reptiles and birds ......................................................... 12 1.4.1 General lay-out ..................................................................................... 12 1.4.2 The pallium in reptiles and birds ........................................................... 14 1.4.3 The pallium in mammals ....................................................................... 14 1.4.4 The question of homology ..................................................................... 15 1.4.5 A brain for (complex) cognition ............................................................. 17 1.5 Aims and hypotheses of this thesis ............................................................. 19 Chapter 2 Dopaminergic innervation reveals a possible primordial NCL-like structure in the Nile crocodile (Crocodylus niloticus) ........ 23 2.1 Introduction ................................................................................................. 25 2.2 Material & Methods ..................................................................................... 27 2.2.1 A note on nomenclature ........................................................................ 27 2.2.1.1 Elaboration on the use of ‘reptiles’ ..................................................... 27 2.2.1.2 Neuroanatomy ................................................................................... 27 2.2.2 Immunohistochemistry .......................................................................... 28 2.2.3 TH-fibre density analysis ....................................................................... 28 2.3 Results ........................................................................................................ 29 2.4 Discussion ................................................................................................... 32 Chapter 3 The dopaminergic innervation of the executive caudal nidopallium; a comparative study of pigeon, chicken, zebra finch and carrion crow................................................................................................ 37 3.1 Introduction ................................................................................................. 39 3.2 Material & Methods ..................................................................................... 43 3.2.1 Animals and tissue preparation ............................................................. 43 3.2.2 Immunohistochemistry .......................................................................... 44 3.2.2.1 Tyrosine Hydroxylase (TH) ................................................................ 44 3.2.2.2 Gallyas silver impregnation ................................................................ 45 3.2.3 Data acquisition .................................................................................... 45 3.2.4 TH-fibre density estimation ................................................................... 46 3.2.5 Close-up analysis ................................................................................. 46 3.3 Results ........................................................................................................ 47 3.3.1 TH+ fibre innervation ............................................................................ 47 3.3.1.1 Pigeon ............................................................................................... 49 3.3.1.2 Chicken ............................................................................................. 52 3.3.1.3 Carrion crow ...................................................................................... 55 3.3.1.4 Zebra finch ........................................................................................ 59 3.3.2 Myelinated trajectory of the dorsal arcopallial tract ................................ 63 3.4 Discussion ................................................................................................... 67 3.4.1 Pigeon .................................................................................................. 67 3.4.2 Chicken................................................................................................. 69 3.4.3 Carrion crow and zebra finch ................................................................ 70 3.4.4 Functions of the NCL modulated by dopamine ..................................... 72 3.4.5 An evolutionary perspective of the caudal nidopallium .......................... 75 Chapter 4 Neurons in the avian brain consume three times less glucose compared to mammals ................................................................... 77 4.1 Introduction ................................................................................................. 79 4.2 Material and methods .................................................................................. 80 4.2.1 Animals & housing ................................................................................ 80 4.2.2 PET measurements .............................................................................. 81 4.2.3 Input function ........................................................................................ 83 4.2.4 Image analysis. ..................................................................................... 83 4.2.5 Kinetic modelling ................................................................................... 84 4.2.6 Statistics ............................................................................................... 86 4.3 Results ........................................................................................................ 86 4.4 Discussion ................................................................................................... 95 4.4.1 Methodological considerations and validation ....................................... 95 4.4.1.1 Lumped constant ............................................................................... 96 4.4.1.2 Route of injection ............................................................................... 96 4.4.1.3 State and brain region ....................................................................... 97 4.4.1.4 Comparison to other bird PET study .................................................
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