Neuromethods 134 Roy V. Sillitoe Editor Extracellular Recording Approaches N euromethods Series Editor Wolfgang Walz University of Saskatchewan Saskatoon, SK, Canada For further volumes: http://www.springer.com/series/7657 Extracellular Recording Approaches Edited by Roy V. Sillitoe Department of Pathology & Immunology and Neuroscience, Baylor College of Medicine, Houston, TX, USA Editor Roy V. Sillitoe Department of Pathology & Immunology and Neuroscience Baylor College of Medicine Houston, TX, USA ISSN 0893-2336 ISSN 1940-6045 (electronic) Neuromethods ISBN 978-1-4939-7548-8 ISBN 978-1-4939-7549-5 (eBook) https://doi.org/10.1007/978-1-4939-7549-5 Library of Congress Control Number: 2017960840 © Springer Science+Business Media, LLC 2018 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. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Printed on acid-free paper This Humana Press imprint is published by Springer Nature The registered company is Springer Science+Business Media, LLC The registered company address is: 233 Spring Street, New York, NY 10013, U.S.A. Preface to the Series Experimental life sciences have two basic foundations: concepts and tools. The Neuromethods series focuses on the tools and techniques unique to the investigation of the nervous system and excitable cells. It will not, however, shortchange the concept side of things as care has been taken to integrate these tools within the context of the concepts and questions under investigation. In this way, the series is unique in that it not only collects protocols but also includes theoretical background information and critiques which led to the methods and their development. Thus it gives the reader a better understanding of the origin of the techniques and their potential future development. The Neuromethods publishing program strikes a balance between recent and exciting developments like those concerning new animal models of disease, imaging, in vivo methods, and more established techniques, including, for example, immunocytochemistry and electrophysiological technologies. New trainees in neurosciences still need a sound footing in these older methods in order to apply a critical approach to their results. Under the guidance of its founders, Alan Boulton and Glen Baker, the Neuromethods series has been a success since its first volume published through Humana Press in 1985. The series continues to flourish through many changes over the years. It is now published under the umbrella of Springer Protocols. While methods involving brain research have changed a lot since the series started, the publishing environment and technology have changed even more radically. Neuromethods has the distinct layout and style of the Springer Protocols program, designed specifically for readability and ease of reference in a laboratory setting. The careful application of methods is potentially the most important step in the process of scientific inquiry. In the past, new methodologies led the way in developing new d isciplines in the biological and medical sciences. For example, physiology emerged out of anatomy in the nineteenth century by harnessing new methods based on the newly d iscovered phenom- enon of electricity. Nowadays, the relationships between disciplines and methods are more complex. Methods are now widely shared between disciplines and research areas. New devel- opments in electronic publishing make it possible for scientists that encounter new methods to quickly find sources of information electronically. The design of individual volumes and chapters in this series takes this new access technology into account. Springer Protocols makes it possible to download single protocols separately. In addition, Springer makes its print-on-demand technology available globally. A print copy can therefore be acquired quickly and for a competitive price anywhere in the world. Saskatoon, SK Wolfgang Walz v Preface There are now many methods available for studying brain function. Among these are various approaches for recording neurons in vivo. The signals may be collected from populations of neurons using electrode arrays, tetrodes, or single electrodes to collect either local field potentials (LFPs) or action potentials from single cells. These various approaches have been fine-tuned in different species for studying specific behaviors. For example, motor behav- iors are heavily studied in mice and rats, but recent work on looming behavior has benefited greatly from studies in locusts, in which brain activity can be examined with precision dur- ing execution of the behavior. Moreover, the use of conditional genetics in vertebrates and invertebrates and optogenetics approaches in rodents has increased the power of manipu- lating neurons and circuits. These different strategies enable researchers to define the causal relationships between neuronal properties in targeted brain areas to distinct behavioral consequences in health and disease. The chapters in this volume of Neuromethods have brought together experts in the field to discuss extracellular recording techniques with two specific goals in mind. The first is to provide a reasonably detailed outline of the methods, including critical steps for success, advantages of the method, and shortcomings to consider with pointers for how to resolve them. The second is to provide an example application where their specific approach has proven particularly useful, and this may include a discussion of how basic biology has been pushed forward or how translational research and clinical diagnoses or treatments have benefitted from the approaches. The contributing author list encompasses a unique balance of investigators from different areas of neuroscience who study different regions of the brain, using different model systems. The models include mouse, rat, zebrafish, fly, worm, and even locust. We have also included one chapter describing the use of extracellular recordings in studies of human cognition. The techniques range from single-unit recordings to tetrodes, multi-electrode arrays, and imaging systems. Importantly, we have also included a chapter on recording in perinatal and early devel- oping rodents, highlighting the key advances that studies of critical periods, which shape brain function, have made. Overall, several major sectors of the systems neuroscience field are repre- sented by including brain regions involved in sensory, motor, and cognitive functions. In summary, this volume will be an invaluable resource because at the heart of the collection is classic extracellular recording, but the authors describe improvements and additions, as well as more modern and novel tools such as optogenetics and multi-channel recording. I have selectively chosen authors who are at the cutting edge of their respective fields. Our wish was to provide readers with the most up-to-date and original applications of the outlined techniques. I am delighted to say that I believe we achieved those goals. With that, I would like to extend my deepest gratitude to each and every author that con- tributed to what I think is a fantastic and unique collection of chapters. I truly appreciate all the hard work that you put into your chapters, and I know that our readers will share my enthusiasm for your masterfully crafted material. Houston, TX, USA Roy V. Sillitoe vii Contents Preface to the Series � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �v Preface � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �vii Contributors � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � xi 1 In Vivo Loose-Patch-Juxtacellular Labeling of Cerebellar Neurons in Mice....... 1 Amanda M. Brown, Joshua J. White, Joy Zhou, Taylor Jefferson, Tao Lin, and Roy V. Sillitoe 2 Targeted Electrophysiological Recordings In Vivo in the Mouse Cerebellum...... 19 Bin Wu and Martijn Schonewille 3 Single-Unit Extracellular Recording from the Cerebellum During Eyeblink Conditioning in Head-Fixed Mice .............................. 39 Shane A. Heiney, Shogo Ohmae, Olivia A. Kim, and Javier F. Medina 4 Multielectrode Arrays for Recording Complex Spike Activity.................. 73 Eric J. Lang 5 Large-Scale Tetrode Recording in the Rodent Hippocampus ................. 87 Xiang Mou and Daoyun Ji 6 A Guide to In Vivo Optogenetic Applications for Cerebellar Studies............ 109 Oscar H. J. Eelkman Rooda and Freek E. Hoebeek 7 A Combinatorial Approach to Circuit Mapping in the Mouse Olfactory Bulb ..... 129 Gary Liu, Jessica Swanson, Brandon Pekarek, Sugi Panneerselvam, Kevin Ung, Burak Tepe, Longwen Huang, and Benjamin R. Arenkiel 8 In Vivo Recordings at the Caenorhabditis elegans Neuromuscular Junction....... 143 Shangbang Gao and Zhitao Hu 9 Electroantennograms (EAGs) and Electroretinograms (ERGs) in the Genetic Dissection of Synaptic Function in Drosophila melanogaster ....... 157 Balaji Krishnan and Yogesh P. Wairkar 10 Combined Two-Photon Calcium Imaging and Single-Ommatidium Visual Stimulation to Study Fine-Scale Retinotopy in Insects.................. 185 Ying Zhu and Fabrizio Gabbiani 11 Extracellular Loose-Patch Recording of Purkinje Cell Activity in Awake Zebrafish and Emergence of Functional Cerebellar Circuit ................... 207 Jui-Yi Hsieh and Diane M. Papazian 12 Recording Extracellular Activity in the Developing Cerebellum of Behaving Rats................................................... 225 Greta Sokoloff and Mark S. Blumberg 13 In Vivo Recordings of Network Activity Using Local Field Potentials and Single Units in Movement and Network Pathophysiology ................ 249 Richard Courtemanche and Maxime Lévesque ix x Contents 14 Surgical and Electrophysiological Techniques for Single-Neuron Recordings in Human Epilepsy Patients .......................................... 267 Juri Minxha, Adam N. Mamelak, and Ueli Rutishauser Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295 Contributors Benjamin R. aRenkiel • Department of Molecular & Human Genetics and Neuroscience, Program in Developmental Biology, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA maRk S. BlumBeRg • Department of Psychological & Brain Sciences, University of Iowa, Iowa City, IA, USA; DeLTA Center, University of Iowa, Iowa City, IA, USA; Interdisciplinary Graduate Program in Neuroscience, University of Iowa, Iowa City, IA, USA; Department of Biology, University of Iowa, Iowa City, IA, USA amanda m. BRown • Department of Pathology & Immunology and Neuroscience, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA RichaRd couRtemanche • Department of Exercise Science & FRQS Groupe de Recherche en Neurobiologie Comportementale/CSBN, Concordia University, Montreal, QC, Canada oScaR h.j. eelkman Rooda • Department of Neuroscience, Erasmus Medical Center, Rotterdam, The Netherlands ShangBang gao • Key Laboratory of Molecular Biophysics of the Ministry of Education, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, China FaBRizio gaBBiani • Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA Shane a. heiney • Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA FReek e. hoeBeek • Department of Neuroscience, Erasmus Medical Center, Rotterdam, The Netherlands jui-yi hSieh • Circuit Therapeutics, Inc�, Menlo Park, CA, USA; Department of Physiology and the Interdepartmental Program in Molecular, Cellular, and Integrative Physiology, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA zhitao hu • Queensland Brain Institute, The University of Queensland, Brisbane, QLD, Australia longwen huang • Department of Neuroscience, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA tayloR jeFFeRSon • Department of Pathology & Immunology and Neuroscience, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA daoyun ji • Department of Molecular & Cellular Biology and Neuroscience, Baylor College of Medicine, Houston, TX, USA olivia a. kim • Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA Balaji kRiShnan • Department of Neurology, Mitchell Center for Neurodegenerative Diseases, University of Texas Medical Branch, Galveston, TX, USA eRic j. lang • Department of Neuroscience & Physiology, New York University School of Medicine, New York, NY, USA xi xii Contributors maxime léveSque • Department of Neurology & Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, QC, Canada tao lin • Department of Pathology & Immunology and Neuroscience, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA gaRy liu • Program in Developmental Biology, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA adam n. mamelak • Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA javieR F. medina • Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA juRi minxha • Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA, USA; Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA xiang mou • Department of Molecular and Cellular Biology and Neuroscience, Baylor College of Medicine, Houston, TX, USA Shogo ohmae • Department of Neuroscience, Baylor College of Medicine, Houston, TX, USA Sugi PanneeRSelvam • Department of Molecular & Human Genetics, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA diane m. PaPazian • Department of Physiology and the Interdepartmental Program in Molecular, Cellular, and Integrative Physiology, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA BRandon PekaRek • Department of Molecular & Human Genetics, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA ueli RutiShauSeR • Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA, USA; Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA; Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA, USA maRtijn Schonewille • Department of Neuroscience, Erasmus Medical Center, Rotterdam, The Netherlands Roy v. Sillitoe • Department of Pathology & Immunology and Neuroscience, Program in Developmental Biology, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA gReta SokoloFF • Department of Psychological & Brain Sciences, University of Iowa, Iowa City, IA, USA; DeLTA Center, University of Iowa, Iowa City, IA, USA jeSSica SwanSon • Department of Molecular & Human Genetics, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA BuRak tePe • Program in Developmental Biology, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA kevin ung • Program in Developmental Biology, Baylor College of Medicine, Jan and Dan Duncan Neurological Research Institute of Texas Children’s Hospital, Houston, TX, USA