Springer Handbook of Auditory Research

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David K. Ryugo ● Richard R. FayArthur N. PopperEditors

Auditory and Vestibular Efferents

ISSN 0947-2657ISBN 978-1-4419-7069-5 e-ISBN 978-1-4419-7070-1DOI 10.1007/978-1-4419-7070-1Springer New York Dordrecht Heidelberg London

Library of Congress Control Number: 2010937633

© Springer Science+Business Media, LLC 2011All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden.The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights.

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Springer is part of Springer Science+Business Media (www.springer.com)

EditorsDavid K. RyugoGarvan Institute of Medical Research Program in Neuroscience 384 Victoria St., Level 7Darlinghurst, NSW 2010Australiad.ryugo@garvan.org.au

Arthur N. PopperUniversity of Maryland Department of BiologyCollege Park, Maryland20742-4415USAapopper@umd.edu

Richard R. FayDepartment of Psychology Loyola University of Chicago 6525 N. Sheridan Rd. Chicago, Illinois 60626USArfay@luc.edu

This volume is dedicated to our families:Kay and Masako Ryugo; Karen, Ben, Dan, and Nick Ryugo

Catherine Fay; Christian and Kara Fay, Amanda Fay, and Nate Evan and Stella Fay

Helen Popper; Michelle, Roman, and Emma Levit; Melissa, Jeff, Ethan, and Sophie Levinsohn

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Series Preface

The Springer Handbook of Auditory Research presents a series of comprehensive and synthetic reviews of the fundamental topics in modern auditory research. The volumes are aimed at all individuals with interests in hearing research including advanced graduate students, post-doctoral researchers, and clinical investigators. The volumes are intended to introduce new investigators to important aspects of hearing science and to help established investigators to better understand the fun-damental theories and data in fields of hearing that they may not normally follow closely.

Each volume presents a particular topic comprehensively, and each serves as a synthetic overview and guide to the literature. As such, the chapters present neither exhaustive data reviews nor original research that has not yet appeared in peer-reviewed journals. The volumes focus on topics that have developed a solid data and conceptual foundation rather than on those for which a literature is only begin-ning to develop. New research areas will be covered on a timely basis in the series as they begin to mature.

Each volume in the series consists of a few substantial chapters on a particular topic. In some cases, the topics will be ones of traditional interest for which there is a substantial body of data and theory, such as auditory neuroanatomy (Vol. 1) and neurophysiology (Vol. 2). Other volumes in the series deal with topics that have begun to mature more recently, such as development, plasticity, and computational models of neural processing. In many cases, the series editors are joined by a co-editor having special expertise in the topic of the volume.

Richard R. Fay, Chicago, ILArthur N. Popper, College Park, MC

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Volume Preface

Research on sensory efferents has entered a renaissance period, particularly with respect to the auditory and vestibular systems. Since the discovery of auditory efferents by Grant Rasmussen, understanding of its significance to sensory process-ing has grown. To accentuate the whole efferent system associated with the ear, this volume covers a wide range of topics addressing the biology of auditory and ves-tibular efferents. Basic research reviews of the anatomy, electrophysiology, and pharmacology lead into discussions of cellular and molecular features of the inner ear. Chapters on the development and evolution of efferent systems illuminate key phylogenetic stages and ontogenetic mechanisms that have given rise to present-day efferent systems. The final chapters provide an overview of central efferent anatomy and neuronal responses and plasticity to efferent activation.

The first chapter by David Ryugo introduces the idea of sensory efferents and explores the concept with respect to biological mechanisms and behavior. The behavioral responses of organisms when confronted by sensory challenges are often best explained by invoking a functioning efferent system. When considering what a nervous system must do, one can design experiments to test hypotheses about what the nervous system actually does. This context sets the stage for the rest of the volume.

Chapter 2 by Chris Brown exploits the basic relationship between structure and function to establish an anatomical foundation for understanding olivocochlear neu-rons. This discussion is followed by a summary of the physiological response prop-erties of the efferent neurons in Chapter 3 by John Guinan. The anatomical distinctions outlined in Chapter 2 are consistent with the different mechanisms uti-lized by the lateral and medial olivocochlear systems to alter cochlear function. The separate olivocochlear systems use different chemical mechanisms that are dis-cussed in detail by Bill Sewell in Chapter 4. Sewell’s introduction to cochlear effer-ent neurochemistry is followed by a consideration of the role of special nicotinic receptors and various ion channels by Eleonora Katz, Ana Belén Elgoyhen, and Paul A. Fuchs in Chapter 5 to explain how acetylcholine mediates fast inhibition.

Chapter 6 by Joseph C. Holt, Anna Lysakowski, and Jay M. Goldberg introduce the vestibular component of inner ear efferents. This update on the current knowl-edge of vestibular efferents emphasizes the complicated nature of the system and hints at new directions and questions.

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Dwayne Simmons, Jeremy Duncan, Dominique Crapon de Caprona, and Bernd Fritzsch review development of the vestibulocochlear efferent system in Chapter 7 and reveal provocative findings that shape our understanding about mechanisms of inner ear development. This treatise is followed by Chapter 8 in which Christine Köppl addresses efferent system diversity in terms of evolutionary concepts.

Chapter 9 by Brett Schofield describes the descending auditory circuitry that forms long descending projections as well as short feedback loops within the cen-tral auditory system. Chapter 10 by Donald Robertson and Wilhelmina Mulders discusses the central effects of efferent activation on physiological response proper-ties of auditory neurons, and Nobuo Suga, Weiqing Ji, Xiaofeng Ma, Jie Tang, Zhongju Xiao, and Jun Yan summarize in Chapter 11 how many forms of brain and behavioral plasticity depend on efferent systems.

As is often the case, chapters in a newer SHAR volume are complemented by, and complimentary to, chapters in earlier volumes. Although there have been few chapters in earlier volumes that were specifically on efferent systems, the issue was critical as parts of chapters in volumes such as The Cochlea (Vol. 8), Integrative Functions in the Mammalian Auditory Pathway (Vol. 15), and The Vestibular System (Vol. 19). In addition, the anatomy of the olivocochlear vestibular system was specifically discussed by W. Bruce Warr in Vol. 1 of this series, The Mammalian Auditory Pathway: Neuroanatomy and by Russell and Lukashkin in Active Processes and Otoacoustic Emissions (Vol. 30).

David Ryugo, Darlinghurst, NSW, AustraliaRichard R. Fay, Chicago, IL

Arthur N. Popper, College Park, MD

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Contents

1 Introduction to Efferent Systems ........................................................... 1David K. Ryugo

2 Anatomy of Olivocochlear Neurons ...................................................... 17M. Christian Brown

3 Physiology of the Medial and Lateral Olivocochlear Systems ............ 39John J. Guinan

4 Pharmacology and Neurochemistry of Olivocochlear Efferents ................................................................................................... 83William F. Sewell

5 Cholinergic Inhibition of Hair Cells ...................................................... 103Eleonora Katz, Ana Belén Elgoyhen, and Paul Albert Fuchs

6 The Efferent Vestibular System ............................................................. 135Joseph C. Holt, Anna Lysakowski, and Jay M. Goldberg

7 Development of the Inner Ear Efferent System ................................... 187Dwayne Simmons, Jeremy Duncan, Dominique Crapon de Caprona, and Bernd Fritzsch

8 Evolution of the Octavolateral Efferent System ................................... 217Christine Köppl

9 Central Descending Auditory Pathways ............................................... 261Brett R. Schofield

10 Central Effects of Efferent Activation .................................................. 291Donald Robertson and Wilhelmina H.A.M. Mulders

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11 Corticofugal Modulation and Beyond for Auditory Signal Processing and Plasticity ............................................................ 313Nobuo Suga, Weiqing Ji, Xiaofeng Ma, Jie Tang, Zhongju Xiao, and Jun Yan

Index ................................................................................................................. 353

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M. Christian Brown Department of Otology and Laryngology, Harvard Medical School, and Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA Chris_Brown@meei.harvard.edu

Dominique Crapon de Caprona Department of Biology, University of Iowa, Iowa City, IA, 52242, USA dominique-decaprona@uiowa.edu

Jeremy Duncan Department of Biology, University of Iowa, Iowa City, IA, 52242, USA jeremy-duncan@uiowa.edu

Ana Belén Elgoyhen Instituto de Investigaciones en Ingeniería Genética y Biología Molecular (Consejo Nacional de Investigaciones Científicas y Técnicas), 1428, Buenos Aires, Argentina elgoyhen@dna.uba.ar

Bernd Fritzsch Department of Biology, University of Iowa, Iowa City, IA 52242, USA bernd-fritzsch@uiowa.edu

Paul Albert Fuchs Department of Otolaryngology, Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA pfuchs@jhmi.edu

Contributors

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Jay M. Goldberg Department of Neurobiology, Pharmacology, and Physiology, University of Chicago, Chicago, IL 60637, USA jgoldber@bsd.uchicago.edu

John J. GuinanJr Eaton Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA Department of Otology and Laryngology, Harvard Medical School, Boston, MA, USA Speech and Hearing Bioscience and Technology Program, Harvard-MIT Division of Health Sciences and Technology, Boston, MA, USA jjg@epl.meei.harvard.edu

Joseph C. Holt Department of Otolaryngology/Neurobiology and Anatomy, University of Rochester, Rochester, NY 14642, USA joseph_holt@urmc.rochester.edu

Weiqing Ji Department of Biology, Washington University, St. Louis, MO 63130, USA ji@biology.wustl.edu

Eleonora Katz Instituto de Investigaciones en Ingeniería Genética y Biología Molecular (Consejo Nacional de Investigaciones Científicas y Técnicas), 1428, Buenos Aires, Argentina ekatz@dna.uba.ar

Christine Köppl Cochlear and Auditory Brainstem Physiology, IBU, Carl von Ossietzky University Oldenburg, 26111, Oldenburg, Germany christine.koeppl@uni-oldenburg.de

Anna Lysakowski Department of Anatomy and Cell Biology, University of Illinois at Chicago, Chicago, IL 60612, USA alysakow@uic.edu

Xiaofeng Ma Department of Biology, Washington University, St. Louis, MO 63130, USA xfma@biology.wustl.edu

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Wilhelmina H.A.M. Mulders The Auditory Laboratory, Discipline of Physiology, M311 School of Biomedical Biomolecular and Chemical Sciences, The University of Western Australia, Crawley, WA 6009, Australia hmulders@cyllene.uwa.edu.au

Donald Robertson The Auditory Laboratory, Discipline of Physiology, M311 School of Biomedical Biomolecular and Chemical Sciences, The University of Western Australia, Crawley, WA 6009, Australia drobed@cyllene.uwa.edu.au

David K. Ryugo Garvan Institute of Medical Research, Program in Neuroscience, 384 Victoria St., Level 7, Darlinghurst, NSW, Australia and Center for Hearing and Balance, 720 Rutland Ave., Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA d.ryugo@garvan.org.au

Brett R. Schofield Department of Anatomy and Neurobiology, Northeastern Ohio Universities Colleges of Medicine and Pharmacy, Rootstown, OH 44272, USA bschofie@neoucom.edu

William F. Sewell Department of Otology and Laryngology, Harvard Medical School, Boston, MA 02114, USA and Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA wfs@epl.meei.harvard.edu

Dwayne Simmons Department of Physiological Science, University of California, Los Angeles, CA, 90095-1606, USA dd.simmons@ucla.edu

Nobuo Suga Department of Biology, Washington University, St. Louis, MO 63130, USA suga@biology.wustl.edu

xvi Contributors

Jie Tang Department of Biology, Washington University, St. Louis, MO 63130, USA ietang@creighton.edu

Zhongju Xiao Department of Physiology, Southern Medical University, Guangzhou 510515, P.R., China Xiaozj@fimmu.com

Jun Yan Department of Physiology and Biophysics, University of Calgary, N.W. Calgary, Alberta, Canada, T2N 4N1 juyan@ucalgary.ca