The Computing Dendrite: From Structure to Function PDF
Preview The Computing Dendrite: From Structure to Function
Springer Series in Computational Neuroscience Hermann Cuntz Michiel W.H. Remme Benjamin Torben-Nielsen E ditors The Computing Dendrite From Structure to Function Springer Series in Computational Neuroscience Volume 11 Series Editors Alain Destexhe Unité de Neuroscience, Information et Complexité (UNIC) CNRS Gif-sur-Yvette France Romain Brette Equipe Audition (ENS/CNRS) Département d’Études Cognitives École Normale Supérieure Paris France For further volumes: http://www.springer.com/series/8164 Hermann Cuntz (cid:129) Michiel W.H. Remme Benjamin Torben-Nielsen Editors The Computing Dendrite From Structure to Function Editors Hermann Cuntz Michiel W.H. Remme Ernst Strüngmann Institute (ESI) Institute for Theoretical Biology for Neuroscience in Cooperation Humboldt-Universität zu Berlin with Max Planck Society Berlin , Germany Frankfurt/Main, Germany Institute of Clinical Neuroanatomy Goethe University Frankfurt/Main, Germany Benjamin Torben-Nielsen Department of Neurobiology Hebrew University of Jerusalem Jerusalem, Israel Blue Brain Project Swiss Federal Institute of Technology in Lausanne Lausanne, Switzerland ISSN 2197-1900 ISSN 2197-1919 (electronic) ISBN 978-1-4614-8093-8 ISBN 978-1-4614-8094-5 (eBook) DOI 10.1007/978-1-4614-8094-5 Springer New York Heidelberg Dordrecht London Library of Congress Control Number: 2013952927 © Springer Science+Business Media New York 2014 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifi cally the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfi lms 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. Exempted from this legal reservation are brief excerpts in connection with reviews or scholarly analysis or material supplied specifi cally for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Duplication of this publication or parts thereof is permitted only under the provisions of the Copyright Law of the Publisher’s location, in its current version, and permission for use must always be obtained from Springer. Permissions for use may be obtained through RightsLink at the Copyright Clearance Center. Violations are liable to prosecution under the respective Copyright Law. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specifi c statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. While the advice and information in this book are believed to be true and accurate at the date of publication, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Printed on acid-free paper Springer is part of Springer Science+Business Media (www.springer.com) Foreword Dendrites have always been there—for hundreds of millions of years—but we became closely familiar with their anatomical esthetics only at the end of the nine- teenth century, following the intellectual fascination and artistic capabilities of sev- eral great anatomists, in particular Santiago Ramón y Cajal and Camillo Golgi. Like the naming of the trees in the forest based on the shape of their crown, many of the names given to neurons rely on the particular shape of the dendritic tree—retinal amacrine cells, cortical spiny stellate cells, and cerebellar Purkinje cells. Naming the trees makes the forest more familiar to us; classifying neurons into anatomical subclasses is a natural path towards “knowing your brain”. Next came the understanding that dendrites serve as the major region of neurons to “accept” their (pre) synaptic partners and that neurons are polygamist, each inter- acting with thousands of other neurons—forming large interactive networks. In 1959, Wilfrid Rall realized that dendrites are electrically distributed devices (rather than an isopotential “point”); this ignited the need to understand how the synaptic current spreads from the synaptic input site to other dendritic regions, in particular to the soma-axon where the output is generated. Rall’s passive cable theory for den- drites has provided the theoretical foundation for this biophysical understanding. The experimental fi nding that the dendritic membrane is endowed with a rich reper- toire of nonlinear voltage- and ligand-gated ion channels, and that synaptic inputs (inhibitory and excitatory) from different input sources target specifi c dendritic sub- domains, suggested that dendrites (and their synapses) may empower neurons with enhanced computational capabilities. With this experimental and theoretical foundation, a new perspective has emerged regarding the possibility that dendrites might implement computational functions. McCulloch and Pitts (1943) inspired this conceptual jump, demonstrating that logi- cal operation could be performed by neurons (with their “all or none” “0” and “1” spikes, and their excitatory and inhibitory synapses). In 1964 Rall showed in a com- putational study that the soma voltage is sensitive to the temporal sequence of syn- aptic activation “swiping” over the dendritic tree, and that this property could be used to perform a fundamental computation—sensitivity to the direction of motion. v vi Foreword This was the fi rst convincing demonstration that dendrites and their synapses could perform elementary computations; it marked the beginning of the 50-year search for “dendritic computation”. Remarkable theoretical ideas were published regarding the role of dendrites in performing specifi c computations, including (1) the detection of motion direction; (2) their key role in collision avoidance; (3) storage and classifi cation of multiple input features; (4) calculation of position variables; (5) recovering input signals in the presence of strong noise; (6) enhancing temporal resolution for coincidence detection. But do dendrites really perform these computations in the behaving brain or are these ungrounded (but nevertheless intellectually valuable) theories? To answer this we need to connect the (e.g., sensory) information impinging on the dendritic tree via its synaptic inputs to the behaviorally relevant information repre- sented by the neuron’s output. If supplemented with knowledge about synaptic loca- tion on dendrites, then we could fully link dendritic structure, synaptic activity/ connectivity to the neuron’s function. Finally with the development of new technological (e.g., new refi ned anatomy available in this age of “connectomics”) and with the inspiration of theories that suggested specifi c mechanisms that might underlie dendritic computation, we are now in a position to directly examine whether dendrites compute. Such direct dem- onstration was fi rst provided by the in vivo study of Single and Borst (1998) and, very recently, additional concrete examples were offered as summarized in the present book. This book is therefore a highly timely refl ection of “dendrites coming of age”; from an anatomical appreciation of dendritic structure (which started 130 years ago and are ongoing) via theoretical ideas about dendritic function(s) (which started 50 years ago and are ongoing), to state-of-the art experimental approaches, enabling for the fi rst time to directly link dendritic electro-anatomical structure, synaptic loci and activity, to the computational functions of dendrites. In his small insightful book (“An Advice to a Young Scientist”) Ramón y Cajal wrote very beautifully the following: “ Basically, the theorist is a lazy person mas- querading as a diligent one. He unconsciously obeys the law of minimum effort because it is easier to fashion a theory than to discover a phenomenon ”. I am confi dent that after reading the present book Cajal would be both totally amazed and inspired by what we have learned about the anatomical, physiological, and molecular secrets that were hidden within the intricacies of h is dendrites . He might also admit that he himself was a theoretician. By proposing the “theory of dynamic polarization” (the direction of signal fl ow from axon-to-dendrites-to-soma-to- axon), he laid the foundations for present-day (and future) theories about informa- tion fl ow in dendrites and about how dendrites process this information—about dendritic computation. On a personal note—it is enchanting for a dendritic person like myself to have such a fresh view on dendrites, as this book offers—a result of a collaborative efforts among an enthusiastic group of young “dendritic lovers” (perhaps inspired by Foreword vii Cajal’s advices to the young). To learn about new developmental principles underlying the unique structure of dendrites, to see experimental validation of ear- lier theoretical ideas, and to realize as emphasized in this book what is still missing, in both theoretical and experimental realms, until dendrites (of both the researcher and those of the experimental system studied) are “forced” to fully expose their secrets. Jerusalem , Israel Idan Segev Pref ace In the spring of 2011, two workshop proposals landed on Idan Segev’s desk: both were virtually identical, suggesting a workshop for the computational neuroscience conference (CNS) in Stockholm later that year. They both proposed a workshop on computational approaches to study dendrites and both asked him, Idan, to give a keynote presentation. Idan brought us together in what was to become the beginning of an ongoing, fruitful collaboration between the three of us, which has presently resulted in the book that lies before you. Our goal with this book was to provide a résumé of the state of the art in experi- mental and theoretical investigations into the functions of dendrites in a variety of neural systems. We are happy that so many authors enthusiastically contributed to this endeavor, resulting in a total of 29 chapters. The book is divided into two parts, each starting with an introductory chapter. The fi rst part of this book focuses on the morphological properties of dendrites and summarizes the approaches to measure dendrite morphology quantitatively and to actually generate synthetic dendrite morphologies in computer models. This mor- phological characterization ranges from studying fractal principles to describe den- drite topologies, to the consequences of optimization principles for dendrite shape. We collected individual approaches to study which aspects of dendrite shape can be related directly to underlying circuit constraints and computation. The second part of this book focuses on how dendrites contribute to the computa- tions that neurons perform. What role do dendritic morphology and the distributions of synapses and membrane properties over the dendritic tree have in determining the output of a neuron in response to its input? We brought together representative stud- ies, with topics ranging from general to system-specifi c phenomena, some having a strong experimental component, and others being completely theoretical. The stud- ies come from many different neural systems and animal species ranging from invertebrates to mammals. With this broad focus we aim to give an overview of the diversity of mechanisms that dendrites can employ to shape neural computations. We would like to emphasize that in all our projects together, our contributions were exactly equal, in fact, we drew straws to decide on the editor order on the cover of this book (which turned out to be alphabetical). We would like to thank all the ix
The list of books you might like
