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Diversity and Commonality in Animals Shuichi Shigeno Yasunori Murakami Tadashi Nomura Editors Brain Evolution by Design From Neural Origin to Cognitive Architecture Diversity and Commonality in Animals Series editors Takahiro Asami Matsumoto, Japan Hiroshi Kajihara Sapporo, Japan Kazuya Kobayashi Hirosaki, Japan Osamu Koizumi Fukuoka, Japan Masaharu Motokawa Kyoto, Japan Kiyoshi Naruse Okazaki, Japan Akiko Satoh Hiroshima, Japan Kazufumi Takamune Kumamoto, Japan Hideaki Takeuchi Okayama, Japan Michiyasu Yoshikuni Fukuoka, Japan The book series Diversity and Commonality in Animals publishes refereed volumes on all aspects of zoology, with a special focus on both common and unique features of biological systems for better understanding of animal biology. Originating from a common ancestor, animals share universal mechanisms, but during the process of evolution, a large variety of animals have acquired their unique morphologies and functions to adapt to the environment in the struggle for existence. Topics covered include taxonomy, behavior, developmental biology, endocrinology, neuroscience, and evolution. The series is an official publication of The Zoological Society of Japan. More information about this series at http://www.springer.com/series/13528 Shuichi Shigeno • Yasunori Murakami • Tadashi Nomura Editors Brain Evolution by Design From Neural Origin to Cognitive Architecture 123 Editors Shuichi Shigeno Yasunori Murakami Stazione Zoologica Anton Dohrn Ehime University Naples, Italy Matsuyama, Japan Tadashi Nomura Kyoto Prefectural University of Medicine Kyoto, Japan ISSN 2509-5536 ISSN 2509-5544 (electronic) Diversity and Commonality in Animals ISBN 978-4-431-56467-6 ISBN 978-4-431-56469-0 (eBook) DOI 10.1007/978-4-431-56469-0 Library of Congress Control Number: 2016962454 © Springer Japan KK 2017 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer Japan KK The registered company address is: Chiyoda First Bldg. East, 3-8-1 Nishi-Kanda, Chiyoda-ku, Tokyo 101-0065, Japan Preface The present book is a new, detailed examination to explain how elegant brains have been shaped by simple principles in evolution. Classic comparative studies have revealed great diversity of neural networks and complex behaviors in many animal groups. The recent integrative molecular, developmental, physiological, and psychological approaches, however, have revealed unexpected commonality in the basic structures and functions across animal phylogeny. The structural frameworks of the nervous systems and brains are often replicated in artificial intelligence or machines constructed by human activities, suggesting that functional similarities provide a common design for information processing systems through biophysical constraints. The book introduces the origin of neurons with the single-cell creatures without neurons and then goes on to primordial types in invertebrates such as cnidarians, flatworms, molluscs, insects, and chordates, with a great abundance of the brains of vertebrates: fish, reptiles, birds, and mammals, including whales and humans. Recently, a number of research investigations of diverse and minor organisms have been conducted, and we need to keep up to date. Each chapter provides professional and detailed topics about brain evolution; however, this book as a whole is arranged along a simple concept to find something of common design. Also, non-organisms such as models and materials are covered to explore the designs in the origin and evolutionary processes, but they are not comprehensive. The topics are provided in a timely manner because novel techniques emerged rapidly, for example, as seen in next-generation sequencers and omics (e.g., genomics, proteomics, metabolomics, and connectomics) approaches. With the explosion of big data, the neural-related genes and molecules are now on the radar. Importantly, now the neural networks have been taken notice of. For instance, Europe’s AC1 billion science and technology projects, such as the Human Brain Project, were launched in 2013 to analyze brain connectomics. The big interdisci- plinary plan, the Blue Brain Project, also aims to understand the small mammalian brain. Furthermore, with the rise of recently advanced artificial neural networks, there is enthusiasm for the development of neural network models. The views of brain evolution provide an essential opportunity to generate ideas for novel neuron- v vi Preface and brain-inspired computation. For that reason, this book will show the reader how to extract meaningful neural structures in nature. For undergraduates, graduate students, and professional scientists who seek a deeper understanding, this volume demonstrates how to find the basic principles shaping brains that provided higher cognitive functions in the course of evolution. Our ambition is that the book will stimulate students, particularly young scientists, to delve into problems remaining in this discipline. Many authors were selected from young Japanese scientists, and this work is part of a series of publications of the Zoological Society of Japan. Naples, Italy Shuichi Shigeno Matsuyama, Japan Yasunori Murakami Kyoto, Japan Tadashi Nomura Contents Part I The Origins of Neurons and Networks 1 Physical Ethology of Unicellular Organisms ............................ 3 Shigeru Kuroda, Seiji Takagi, Tetsu Saigusa, and Toshiyuki Nakagaki 2 Molecular Characteristics of Neuron-like Functions in Single-Cell Organisms .................................................. 25 Shingo Maegawa 3 Back Through Time: How Cnidarians and Basal Metazoans Shed Light on Ancient Nervous Systems ................... 45 Hiroshi Watanabe Part II The Rise of Diverse Brain Types 4 Functional Specification of a Primitive Bilaterian Brain in Planarians ................................................................ 79 Takeshi Inoue 5 The Computation and Robustness of the Mini-Cognitive Centers of Terrestrial Mollusks: An Exquisite Outcome of Brain Evolution .......................................................... 101 Ryota Matsuo 6 Insect Brains: Minute Structures Controlling Complex Behaviors ... 123 Michiyo Kinoshita and Uwe Homberg 7 Identifying Vertebrate Brain Prototypes in Deuterostomes............ 153 Takehiro G. Kusakabe 8 Genome and Transcriptome-Wide Research of Brain Evolution ..... 187 Atsushi Ogura vii viii Contents Part III Cognitive Systems 9 The Origin of Vertebrate Brain Centers ................................. 215 Yasunori Murakami 10 Adaptive Radiation and Vertebrate Brain Diversity: Cases of Teleosts.................................................................... 253 Naoyuki Yamamoto 11 Molecular Profiling Reveals Insight into Avian Brain Organization and Functional Columnar Commonalities with Mammals .............................................................. 273 Kazuhiro Wada, Chun-Chun Chen, and Erich D. Jarvis 12 The Neocortex and Dorsal Ventricular Ridge: Functional Convergence and Underlying Developmental Mechanisms ............ 291 Wataru Yamashita and Tadashi Nomura 13 Molecular Investigations of the Structure and Development of the Brain of Carnivores ............................ 311 Yohei Shinmyo, Tomohisa Toda, Kosuke Masuda, Yoshio Hoshiba, Haruka Ebisu, Naoyuki Matsumoto, and Hiroshi Kawasaki 14 Evolution of the Mammalian Brain with a Focus on the Whale Olfactory Bulb .............................................. 329 Takushi Kishida 15 The Evolution and Function of Sleep..................................... 343 Yu Hayashi and Chih-Yao Liu 16 Prefrontal Anatomical Architecture and Top-Down Behavioral Control in Human and Nonhuman Primates .............. 367 Yosuke Morishima Part IV Models and Designs 17 Organisational Principles of Connectomes: Changes During Evolution and Development ...................................... 387 Roman Bauer and Marcus Kaiser 18 Muscular-Hydrostat Computers: Physical Reservoir Computing for Octopus-Inspired Soft Robots........................... 403 Kohei Nakajima 19 Brain Evolution as an Information Flow Designer: The Ground Architecture for Biological and Artificial General Intelligence .................................................................. 415 Shuichi Shigeno Part I The Origins of Neurons and Networks Chapter 1 Physical Ethology of Unicellular Organisms Shigeru Kuroda, Seiji Takagi, Tetsu Saigusa, and Toshiyuki Nakagaki Abstract In this chapter, some behaviours of unicellular