Synaptic Modifications and Memory: An Electrophysiological Analysis

314 Pages·1993·13.665 MB·English

by  Professor Dr. Leon L. Voronin (auth.)

WITHDRAWN BY THE
UNIVERSITY OF MICHIGAN LIBRARY
Studies of Brain Function Vol. 19
Coordinating Editor
V. Braitenberg, Tiibingen
Editors
H. B. Barlow, Cambridge
T. H. Bullock, La Jolla
E. Florey, Konstanz
O.-J. GrOsser, Berlin
A. Peters, Boston
Leon L. Voronin
Synaptic Modifications
and Memory
An Electrophysiological Analysis
With 64 Figures
Springer-Verlag
Berlin Heidelberg New York
London Paris Tokyo
Hong Kong Barcelona
Budapest
Professor Dr. LEON L. VORONIN
Brain Research Institute
Russian Academy of Medical Sciences
Per Obukha 5
Moscow 103064
Russia
ISBN-13: 978-3-642-47619-8 e-ISBN-13: 978-3-642-47615-0
DOl: 10.1007/978-3-642-47615-0
Library of Congress Cataloging-in-Publication Data. Voronin, L. L. Synaptic modifications and
memory: an electrophysiological analysis I Leon L. Voronin. p. em. - (Studies of brain function;
vol. 19) Includes bibliographical references and index. ISBN-13: 978-3-642-47619-8
1. Neuroplasticity. 2. Hippocampus (Brain) 3. Memory. I. Title. II.
Series: Studies of brain function; v. 19. [DNLM: 1. Electrophysiology. 2. Memory - physiology.
3. Hippocampus - physiology. 4. Receptors, Synaptic - physiology. WI ST937KF v. 19 1993 I
WL 102 V9535s 1993] QP364.V67 1993 153.1'2-dc20 DNLM/DLC for Library of Congress
93-6851
This work is subject to copyright. All rights are reserved, whether the whole or part of the material
is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microfilm or in any other way, and storage in data banks. Duplica
tion of this publication or parts thereof is permitted only under the provisions of the German
Copyright Law of September 9, 1965, in its current version, and permission for use must always
be obtained from Springer-Verlag. Violations are liable for prosecution under the German
Copyright Law.
© Springer-Verlag Berlin Heidelberg 1993
Softcover reprint of the hardcover I st edition 1993
The use of general descriptive names, registered names, trademarks, 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.
Media conversion: M. Masson-Scheurer, Kirkel
3113145-5 4 3 2 1 0 - Printed on acid-free paper
Acknowledgements
Several scientific meetings and several persons are related to the initia
tion of this monograph. At the end of 1985, following a talk at the Max
Planck-Institute for Biological Cybernetics in Tiibingen, Professor Dr.
Valentino Braitenberg proposed that I write a book for his series, Studies
of Brain Function. I accepted this kind proposal, having in mind some
initial experience in summarizing earlier results of our group both in a
monograph edited by Georgian Academician Tengiz Oniani [1015] and
in reviews [1012, 1016, 1017] sponsored by Academician Platon
Kostyuk, the Editor-in-Chief of Neurophysiology and Neuroscience. The
cooperation with Dr. Ulrich Kuhnt from Gl>ttingen which started in 1986
following "perestroika" events was of incomparable value both for com
pleting a certain stage in our studies of L1 P mechanisms and writing the
monograph. Very stimulating were invitations of Drs. Helmut Haas and
GyOrgy Buzsaki to participate in a hippocampal meeting in 1987 [1022],
of Hinrich Rahmann to present a review of LT P studies at a meeting in
Mainz in 1988 [1023], of William H. Gispen and Steven Rose to partici
pate in meetings on learning and memory in 1989 and 1990, and of Jan
Delacour to write a review chapter on hippocampal L1 P for his book on
memory mechanisms in 1991. These and several other meetings and dis
cussions with many scientists from East and West were very useful and
encouraging. Last, but not least, were two invitations of Valentino
Braitenberg to Tiibingen in 1991 where I essentially completed the
writing of the manuscript with his generous support and advice. I
initiated the writing of the monograph with the hope that the cooperation
with Western scientists and a more precise knowledge of Russian science
would serve not only purely scientific purposes but would also further a
closer mutual understanding between different nations, thus contributing
to peace on this planet.
I would like to thank all those who directly or indirectly contributed
to this monograph. It is difficult to list all the names and I confine myself
to expressing gratitude to my colleagues who participated in ex
periments, data processing, discussions and writing of related original
publications. Thanks are due to the following for their generosity in giv
ing permission to use the materials on which an essential part of this
book is based: Drs. A. Baskys (Chaps. I, 8, 11, 12), I. E. Kudryashov
(Chaps. 1, 3-6, 8, 11), S. L. Buldakova (Chap. 1) and I. N. Sharonova
VI Acknowledgements
(Chaps. 1, 3), Professor Dr. V. G. Skrebitsky (Chaps. 1,3), Drs. L. N.
Gusev, V. S. Kesarev, D. R. Shidarev, V. F. Uvarov (Chap. 3), R. G.
Kozhedub and S. N. Kozhechkin (Chap. 6), V. I. Derevyagin (Chaps.
8-11), D. B. Logunov (Chaps. 8, 10), G. Hess (Chap. 11, 13, 14), A. G.
Gusev (Chaps. 12, 13-15) and V. Roschin (Chap. 13). I am especially
obliged to Dr. Ulrich Kuhnt for very stimulating cooperation, resulting in
our joint writing of the last experimental Chapters 13-15. I am indebted
to Professors O. S. Adrianov, V. G. Skrebitsky and the late Professor M.
Ya. Rabinovich for encouragement and advice during the experimental
work, as well as in the preparation of the monograph. I am deeply grate
ful to Valentino Braitenberg and Ulrich Kuhnt who took great trouble in
editing the monograph.
Several people gave generous help and advice during the preparation
of the manuscript with word processors. I am grateful to Dieter Michael,
Ludwig Ehrenreich, Anna T1ustochowski, Victor Istomin, Sergei
Molotkov and Nadezhda Nakhutina. I am especially grateful to Mar
garete Ghasroladashti, Hubert Preissl, Thomas Schillen and Igor Chizh
makov for their generous help at the most difficult final stage of the
manuscript preparation. Finally, I cannot find the words to describe my
gratitude to my wife, Eleonora Voronina, for her understanding of my
interest in science and for entering an essential part of the following text
into the computer.
Leon L. Voronin
Contents
Introduction 1
1 Hippocampal Long-Term Potentiation
and Its Characteristics . . . . . . . . . . . . . . 5
1.1 Brief Overview of the Structure of the Hippocampus 5
1.2 Electrical Responses of the Hippocampus 6
1.3 Initial Experiments on Long-Term Potentiation 8
1.4 Working Hypothesis and Early Results 9
1.5 Methods .............. 9
1.6 Long-Term Potentiation of Field Potentials
in the CA3 and CA 1 Regions ..... 10
1.7 Low-Frequency Depression and Self-Restoration
of the Potentiated Response .... 12
1.8 Specificity of Long-Term Potentiation
for the Tetanized Input ..... 14
1.9 Involvement of Reinforcing Systems
During Tetanization 15
1.1 0 Discussion 17
1.11 Summary .... 23
2 Unitary and Minimal Postsynaptic Potentials
(Literature Review) .......... . . .. 25
2.1 Introduction .............. . . .. 25
2.2 Methods Related to Unitary and Minimal PSP Recording 26
2.2.1 Intracellular Stimulation of the Afferent Unit 26
2.2.2 Macrostimulation of Afferent Fibres 26
2.2.3 Intracerebral Microstimulation . . . . . 27
2.2.4 Recording of "Minimal" PSPs .. 27
2.2.5 Additional Procedures for the Detection
of Single UPSPs .......... 28
2.2.6 Measurements of UPSPs and MPSPs Amplitudes
and PSCs . . . . . . . .. .. 28
2.2.7 Mono- and Polysynaptic UPSPs . . . . 29
2.3 Unitary Field Potentials - "EEG Quanta" . . 30
2.4 Applications of Unitary and Minimal PSP Recordings 31
2.4.1 Organization of Neuronal Connections 31
VIII Contents
2.4.2 Electrical and Chemical Synapses in the CNS 31
2.4.3 Spatial Organization of Synapses
on the Somadendritic Membrane .... 32
2.5 Studies of Synaptic Plasticity in the CNS 33
2.5.1 Introductory Remarks . . . . . . . . . 33
2.5.2 Habituation and Sensitization in Invertebrate CNSs 33
2.5.3 Conditioning Mechanisms in the Aplysia CNS 34
2.5.4 LFD in the Vertebrate CNS 35
2.6 Conclusions 35
2.7 Summary ........ . 36
3 "Minimal" Field Potentials ofthe Hippocampus
and Their Post-Tetanic Changes 38
3.1 Introduction .. . . . . . . . . . . . . 38
3.2 Methods .. . .......... . 38
3.3 Field Potentials Correlated with Neuronal Discharges
from the Contralateral Hippocampus . . . . . . . . 39
3.4 Field Activity After Spikes of the Schaffer Collaterals 40
3.5 Minimal Field Potentials ..... . 41
3.6 Post-Tetanic Changes of Minimal FPs 43
3.7 Discussion 43
3.8 Summary ........ . 46
4 Excitatory Postsynaptic Potentials of Hippocampal
Neurones and Their Low-Frequency Depression 47
4.1 Introduction .. . . 47
4.2 Methods .. . . . . .. .. 47
4.3 Responses to Single Stimuli ....... . 49
4.4 Responses to Paired Stimuli of Different Amplitudes 50
4.5 Changes of EPSPs During Low-Frequency Stimulation 52
4.6 Changes of IPSPs During Low-Frequency Stimulation 53
4.7 Discussion 53
4.8 Summary . . . . . .. . ..... 56
5 Responses of Hippocampal Neurones
During Long-Term Potentiation 58
5.1 Introduction . . . . . . . 58
5.2 Methods .. . ..... 58
5.3 General Description of Neuronal Responses 58
5.4 Short-Term Post-Tetanic Changes .. 60
5.5 Long-Term Changes in Spike Responses
after Tetanization .. .... .. 60
5.6 Post-Tetanic Changes of Postsynaptic Potentials 60
5.7 Post-Tetanic Changes in Excitability
and Resting Membrane Potential ...... . 64
Contents IX
5.8 Discussion 65
5.9 Summary 66
6 Changes in Acetylcholine Sensitivity
During Long-Term Potentiation .. 68
6.1 Introduction .......... . 68
6.2 Effects of Acetylcholine Iontophoresis
on Cellular and Field Responses .. 70
6.3 Changes in ACh Sensitivity During L TP 73
6.4 Discussion 75
6.5 Summary .. . ........ . 78
7 Quantal Analysis of Postsynaptic Potentials
(Literature Review) ...... . 79
7.1 Introduction .... ........ . 79
7.2 Principles of the Quantum Hypothesis .. 79
7.3 Methods of Determination of the Mean Quantal Content 81
7.3.1 Direct Counting of Quantal Contents of Single PSPs 81
7.3.2 The Method of "Miniatures" 81
7.3.3 Histogram Method . . . . . 82
7.3.4 Method of Failures . . . . . . . 82
7.3.5 Method of the Coefficient of Variation 83
7.3.6 Analysis of Dispersions 83
7.3.7 Deconvolution Technique . . . . . . 84
7.3.8 Other Methods ....... .. 85
7.4 Corrections for the Methods of Estimating m 85
7.4.1 Non-Linear Summation 85
7.4.2 Control of Steady State 86
7.4.3 "Non-Specific" Activity 86
7.4.4 Multicomponent Miniature PSPs 87
7.4.5 Additional Remarks .. .. 87
7.5 Poisson and Binomial Distributions of PSP Amplitudes 88
7.6 Methods of Estimating Binomial Parameter p 88
7.6.1 Variance of Quantal Distribution ... 88
7.6.2 Variances of Amplitudes of PSPs and mPSPs 88
7.6.3 Division of Amplitude Histogram According to 11 89
7.6.4 Automatic Computation when v Is Known 89
7.6.5 Automatic Analysis of Amplitude Distributions 89
7.6.6 Combination of Variance and Failures Methods 89
7.6.7 Other Methods ..... . 90
7.7 Additional Explanations
to Methods of Computing Quantal Parameters 90
7.7.1 Non-Stationarity and Non-Uniformity 90
7.7.2 Models with Non-Uniform p 91
7.7.3 Other Modifications 92
X Contents
7.8 Basic Quantal Parameters for Various Junctions 92
7.8.1 Neuromuscular Junctions and Autonomic Ganglia 92
7.8.2 Invertebrate CNS 93
7.8.3 Spinal Cord . 94
7.8.4 Cerebrum .... 95
7.8.5 Hippocampus . . 96
7.9 Binomial Parameters n and p for Various Junctions 97
7.9.1 Neuromuscular Junctions and Autonomic Ganglia 97
7.9.2 Invertebrate CNS 98
7.9.3 Spinal Cord . . . . . . . . . . . . . 98
7.9.4 Cerebrum ............. . 99
7.10 Quantal Analysis of Synaptic Plasticity 99
7.10.1 Various Applications of Quantal Analysis 99
7.10.2 Frequency Facilitation (FF) 100
7.10.3 Frequency Depression (FD) ..... 101
7.10.4 Post-Tetanic Potentiation (PTP)
and Heterosynaptic Facilitation (HSF) 102
7.10.5 Long-Term Facilitation (LTF) 103
7.11 Conclusions 104
7.12 Summary ......... . 105
8 Application of Quantal Analysis to Central Synapses 107
8.1 Introduction ................. . 107
8.2 Methods ................... . 107
8.3 Consideration of Known Methods of Determination
of Quantal Parameters .. . 108
8.4 The Histogram Method ..... . 110
8.5 Method Based on the Ratio
of the Mean to Maximal Amplitude 112
8.6 Quantal Parameters of Unitary EPSPs of Snail CNS 113
8.7 Theoretical Distributions of PSP Amplitudes 117
8.8 Discussion 119
8.9 Summary ................ . 122
9 Models of Transmitter Depletion and Their Application
to Analysis of Synaptic Plasticity (Literature Review) 124
9.1 Introduction .................... 124
9.2 Basic Model Parameters and Recording Conditions .. 124
9.3 Model of Transmitter Depletion Without Mobilization 125
9.3.1 Method of Paired Stimulation ........... 125
9.3.2 Method of Amplitude Dependence on Serial Stimulus
Number During Frequency Stimulation 126
9.3.3 Method of Relationship Between Amplitude
and Sum of Amplitudes of Previous Responses 127
9.4 Model of Transmitter Depletion with Mobilization 127