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 ELECTRICAL DYNAMICS OF THE DENDRITIC SPACE

The authors explain how the whole dendtritic arborization contributes to the gen-
eration of various output discharges and elucidate the mechanisms of the transfer
function of all dendritic sites. Their alternative approach to conventional models
introduces the notion of a functional dendritic space, and they have concentrated
on a detailed spatial description of the electrical states at all dendritic sites when
the dendrites operate. By analyzing the electrical dendritic space in which all the
signals are processed, the authors provide tools to explore the spatial dimension
of the transient events well known by electrophysiologists. They demonstrate the
mechanisms by which the operating dendrites decide how, in fine, the distributed
synaptic inputs generate various final output discharges. Their approach reveals
the mechanisms by which individual dendritic geometry determines the sequence
of action potentials that is the neuronal code. An accompanying NeuronViewer
allows readers to monitor the simulation of operating dendritic arborization.

sergey m. korogod is Professor and Head of Department of Experimen-

tal Physics at Dnipropetrovsk National University, and Head of Dnipropetrovsk
Division, International Center for Molecular Physiology at the National Academy
of Sciences of the Ukraine. He explores biophysical mechanisms relating cellular
physical–chemical processes and geometry.
suzanne ty č-dumont is Director of Research Emeritus at CNRS, Paris. She
has been active since the early 1980s in the promotion of the notion of the dendritic
shape as one of the most critical factors in the understanding of dendritic process-
ing, and introduced computational tools for the quantification of the geometry of
dendritic arborizations in her laboratory.
ELECTRICAL DYNAMICS OF THE
DENDRITIC SPACE

SERGEY M. KOROGOD

SUZANNE TY Č-DUMONT
 cambridge university press
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo, Delhi
Cambridge University Press
The Edinburgh Building, Cambridge CB2 8RU, UK

Published in the United States of America by Cambridge University Press, New York

www.cambridge.org
Information on this title: www.cambridge.org/9780521896771

C S. M. Korogod and S. Tyč-Dumont 2009

This publication is in copyright. Subject to statutory exception

and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without
the written permission of Cambridge University Press.

First published 2009

Printed in the United Kingdom at the University Press, Cambridge

A catalogue record for this publication is available from the British Library

ISBN 978-0-521-89677-1 hardback

Cambridge University Press has no responsibility for the persistence or

accuracy of URLs for external or third-party internet websites referred to
in this publication, and does not guarantee that any content on such
websites is, or will remain, accurate or appropriate.
 Contents

Preface page ix
1 Definition of the neuron 1
1.1 The biologist 1
1.2 The physicist 8
1.3 The physicist and the biologist 9
References 10
2 3D geometry of dendritic arborizations 13
2.1 Brief historical background 13
2.2 Single neuron labelling 15
2.3 Dendritic quantification 17
2.4 Data quality and morphological noise 22
2.5 Models of neurons 25
References 31
3 Basics in bioelectricity 37
3.1 Ions as carriers of current 37
3.2 Selective ion permeability of neuronal membrane 38
3.3 Ion pumps 39
3.4 Ion channels 40
3.5 Voltage dependence of membrane conductance 41
3.6 Effective equilibrium potential of multicomponent ion current 41
3.7 Membrane capacitance and capacitive current 42
3.8 External sources 43
3.9 Local current–voltage (I–V) relations 43
Reference 46
4 Cable theory and dendrites 47
4.1 Dendrites as electrical cables 47
4.2 The cable equation 49
4.3 Additional conditions required for solution 53

v
vi Contents

4.4 Input–output (point-to-point) relations in dendritic cables 56

References 57
5 Voltage transfer over dendrites 59
5.1 Dendritic cables in the steady state 59
5.2 Voltage transients in dendritic cables 62
6 Current transfer over dendrites 65
6.1 Charge transfer ratio 65
6.2 Somatopetal current transfer and somatofugal voltage spread 66
6.3 Current transfer ratio for passive paths at different
boundary conditions 71
6.4 Local electro-geometrical coupling in non-uniform paths 72
6.5 Current transfer from distributed dendritic sources 75
References 76
7 Electrical structure of an artificial dendritic path 77
7.1 Electrical structure of passive paths with single-site inputs 79
7.2 Electrical structure of paths with distributed tonic inputs 81
References 94
8 Electrical structure of a bifurcation 95
8.1 Theory for different configurations 95
8.2 Electrical structure of passive branching paths with
single-site inputs 100
8.3 Electrical structure of a bifurcation receiving distributed
tonic inputs 102
8.4 Recapitulation and conclusions 111
References 112
9 Geography of the dendritic space 113
9.1 Dendritic arborization in 3D and 2D representations 114
9.2 Distinct 3D dendritic landscapes 118
9.3 Digitized dendritic arborizations 121
References 125
10 Electrical structures of biological dendrites 127
10.1 Geometry of an example dendrite 127
10.2 Passive dendrite with single-site inputs 129
10.3 Dendrites with distributed inputs 130
10.4 Reconfigurations of passive electrical structures 136
References 139
11 Electrical structure of the whole arborization 141
11.1 Organization of the spatial electrical profiles 141
11.2 Robustness of the electrical bundles 150
11.3 Dynamic reconfigurations of the whole electrical structure 152
 Contents vii

11.4 Spatial aspects of reconfigured electrical structure 156

11.5 Complexity of the whole arborization and its electrical domains 159
References 160
12 Electrical structures in 3D dendritic space 161
12.1 The 3D electrical structures of Purkinje neurons 162
12.2 The 3D electrical structure of pyramidal neurons 164
12.3 The 3D electrical structures of motoneurons 164
12.4 High-efficiency domain of the motoneuronal arborizations
in 3D 166
12.5 Bistable dendritic field 168
References 171
13 Dendritic space as a coder of the temporal output patterns 173
13.1 Terminology to describe the repertoire of neuronal discharges 173
13.2 Geometry-induced features of Purkinje cell discharges 174
13.3 Geometry-dependent repertoire of pyramidal cell activity 189
13.4 Some general rules 193
References 194
14 Concluding remarks 197
14.1 Impact for interpretation of neuronal discharges 199
14.2 The dancing dendrites 200
14.3 Speculation for the future 200
References 202
Index 205
Colour plate section is between pages 116–17.
 Preface

Dear Reader,
We invite you to travel in space with us! This will be a very peculiar space: the den-
dritic space of neurons that is the cosmos for neuroscientists. It is mysterious and
practically unexplored like the outer space we glimpse at in the sky. Curiously, we
can further extend this analogy: the tools of astronomy can be turned from the sky
to the microscope stage to explore shining brain stars, the neurons radiating their
dendrites into the surrounding space. This was performed in the pioneering work
by Paul Gogan and co-workers using a modified astronomical camera to image the
microstructure of the dendritic membrane during the excitation of single live neu-
rons in culture (see references in Chapter 14). The explorers of the dendritic space
still have to invent the appropriate spacecrafts and technologies. As in cosmology,
experimentation is limited, and mathematical and computer models are the only
way of gaining insight into the nature of the dendritic space. The itinerary of our
travel relies on these tools.
We start with a brief historical background to the dendritic problem and describe
the origin of the structural data used for further morphometric and computer simu-
lation studies of the dendritic arborizations (Chapters 1 and 2). Chapter 3 describes
basic bioelectricity with emphasis on space. We show how charge carriers are sep-
arated in space and thus electric fields and currents are created across the neuronal
membrane. An important generalization is that, despite multiplicity and diversity of
channel types, the number of different types of current–voltage relations is restricted
to three. Chapter 4 recapitulates the cable theory of the dendritic transfer properties
with special focus on the terms of the cable equation which determine the electrical
communication across the membrane and along the dendritic membrane. This issue
is further developed in Chapters 5 and 6, specifying the voltage and current transfer
along the dendrites. We highlight that the transfer maps provide an informative
representation of the dendritic electrical structure. Chapters 7 and 8 explain how
the electrical structures of an artificial dendritic path and of a branch bifurcation

ix
x Preface

are built and how they indicate electrical relations in different dimensions of the
dendritic space that are the proximal-to-distal and the path-to-path relations. Next
the critical role of metrical asymmetry of the dendritic branches becomes obvious.
Chapter 9 navigates in the dendritic space of biological neurons and introduces our
library of reconstructed cells providing specific examples of metrical asymmetry
of complex dendritic arborizations. Chapter 10 explores the electrical structures
of single biological dendrites as the basic elements for constructing the whole ar-
borization. Here electrical features related to elementary structural heterogeneities
present in random combinations in the biological dendrites are noticeable. The
electrical structures of the whole reconstructed dendritic arborizations of different
types of neurons are analyzed and classified in Chapters 11 and 12. Relations of the
electrical structures related to size, complexity and asymmetry of the arborizations
are explored. Finally, Chapter 13 considers the consequences of morphological
and electrical structures of the dendritic arborizations for the generation of output
discharge patterns. These spatial–temporal patterns indicate some new emerging
rules by which the dendrites govern the whole cell activity.
This book results from more than 15 years of cooperation between French and
Ukrainian laboratories: the Unit of Cellular Neurocybernetics of the CNRS in
Marseille and the Laboratory of Biophysics and Bioelectronics, Dnipropetrovsk
National University and Dnipropetrovsk Division of the International Center for
Molecular Physiology, National Academy of Sciences of the Ukraine. It originated
in the form of seminars, lectures, published papers and notes for students. We
have benefited from innumerable discussions with students and colleagues. To
acknowledge all of them personally is impossible but we wish to thank first our
collaborators who have co-authored our published articles and who were directly
involved in various aspects of our work at different periods between 1993 and 2007.
This book would have never happened without them.
In the French team, we are specially grateful to Dr. Cesira Batini and Dr.
Ginette Bossavit. We should like to pay tribute to Paul Gogan who initiated the
quantification of dendritic geometry. His vision was far in advance of the impact of
computer science in biology. He had foreseen what could be done by introducing
high computational technology in our neurobiological laboratory. His knowledge
of electrophysiology, his wide scientific background and his generous participation
in our work make him an essential person to thank. We would also like to thank
the technicians, secretaries, programmers and photographers of our laboratories for
their generous assistance and invaluable help.
In the Ukrainian team, Yuri Ivanov, Irina Kopysova and Vladimir Sarana valuably
participated at earlier stages of our joint work on the dendritic processing. We
especially acknowledge the contribution of Dr. Iryna Kulagina, who is the co-
author of most of the results presented in this book, some of which have already
 Preface xi

been published, as well as unpublished data in Chapter 13. Her thorough and
creative work provided novel dynamic electrical maps of the dendritic space which
look sunny and bear clear landmarks of the determinative role of geometry in
spatial–temporal electrical phenomena in the dendrites. We appreciate the creative
contribution by Valery Kukushka who developed the NeuronViewer, a tool for
interactively displaying spatial–temporal dendritic activity described in Chapter 13.
NeuronViewer is available at Cambridge University Press site (URL . . .). Scientific
cooperation between our teams was efficiently supported by the French Embassy
in Ukraine and we are deeply grateful for that.
We want to thank our friends and colleagues Dr. Elska Jankowska, Dr. John
Lagnado, Dr. Bob Liberman, Dr. Hans Lüscher and Dr. Gerta Vrbova for reading
some parts of the manuscript and for their comments, criticisms and encouragement.
Finally and importantly, we regret that we can only provide an incomplete picture
of dendritic spatial processing, but we are happy to open this space for younger
generations of researchers.
 1
Definition of the neuron

1.1 The biologist

The shapes of the dendritic arborization of vertebrate neurons is a unique property
which differentiates the nervous tissue from all the other tissues of the organism.
The neuron doctrine, which we owe to Santiago Ramón y Cajal (Ramón y Cajal,
1904, 1911), was established 50 years after the cellular theory proposed by Schwann
in 1839. This long period of trial and error and of vigourous opposition by the ad-
herents of the reticularism is simply explained by the great difficulty of recognizing
a nerve cell on histological preparations (Figure 1.1).
It was only after the discovery of the Golgi method, which is a selective technique
for visualizing nerve cells and their prolongations that Ramón y Cajal established
the first fundamental concept of neuroscience:

All becomes clear in our minds. Why do dendritic arborizations exist, why are they so
varied, so abundant, so extensive? We understand now. Simply to enable the cell to receive,
and to transmit to its cylinder-axis, the greatest possible variety of signals, from as many
different sources as possible; put simply, to make of the cell a microcosm whose connections
to the interior and exterior worlds are as numerous and complex as possible.

He called the nervous tissue the most intricate structure known in the living
world. He observed a great number of neurons stained with the Golgi method in a
variety of species. The comparison of dendritic morphologies of neurons located
in homologous regions of the brains of different animals led him to formulate what
we call the ‘shape hypothesis’. It was in the darwinism context of the time and
tuned with the comparative phylogenetic approach. During evolution, the structural
complexity of the dendritic arborization is greatly increased and he also illustrated
the idea that the ontogenetic history of a neuron replicates its phylogenetic history
(Figure 1.2).
The evolutionary aspects of the shapes of cellular structures were also studied
in the Moscow Brain Institute, where the concept that the higher we ascend the

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