Table Of ContentH. L. Haas G. Buzsaki (Eds.)
Synaptic Plasticity
in the Hippocampus
Foreword by E. Grastyan
With 55 Figures and 3 Tables
Springer-Verlag Berlin Heidelberg New York
London Paris Tokyo
Professor Helmut L. Haas, M. D.
II. Physiologisches Institut
Johannes Gutenberg-Universitat
Saarstrasse 21,6500 Mainz
Federal Republic of Germany
Professor Gyorgy Buzsaki, M. D.
Department of Neurosciences M024
University of California at San Diego
La Jolla, CA 92093, USA
ISBN-13: 978-3-642-73204-1 e-ISBN-13: 978-3-642-73202-7
001: 10.1007/978-3-642-73202-7
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Foreword
This is the second time that I have had the honor of opening an interna
tional symposium dedicated to the functions of the hippocampus here in
Pecs. It was a pleasure to greet the participants in the hope that their
valuable contributions will make this meeting a tradition in this town.
As one of the hosts of the symposium, I had the sorrowful duty to
remind you of the absence of a dear colleague, Professor Graham God
dard. His tragic and untimely death represents the irreparable loss of
both a friend and an excellent researcher. This symposium is dedicated
to his memory.
If I compare the topics of the lectures of this symposium with those of
the previous one, a striking difference becomes apparent. A dominating
tendency of the previous symposium was to attempt to define hippocam
pal function or to offer data relevant to supporting or rejecting existing
theoretical positions. No such tendency is reflected in the titles of the
present symposium, in which most of the contributions deal with hip
pocampal phenomena at the most elementary level. Electrical, biochemi
cal, biophysical, and pharmacological events at the synaptic, membrane,
or intracellular level are analyzed without raising the question of what
kind of integral functions these elementary phenomena are a part of.
What might be the cause of this theoretical indifference? Perhaps disap
pOintment with the inefficiency of the theoretical debates of more than
three decades? Or the recognition that our knowledge of intrahippocam
pal information processing is still inadequate for verification of func
tional theories? Most of the theoreticians, faithfully following the tradi
tions of functional localization were looking for a single, exclusive func
tion, like orienting, attention, internal inhibition, spatial mapping, work
ing memory, etc. The feasibility of such an approach would now be
questioned by many. Though highly simplistic, it is tempting to make the
assumption that the unique macroscopic shape of the hippocampus,
resembling a seahorse, or its orderly inner organization, resembling
random access memory, might have been suggestive of an exclusive and
unitary function. In the course of my own speculations about hippocam
pal function, whenever a plausible hypothesis emerged I could not ban
ish from my mind the embarrassing clinical evidence that humans with a
complete inborn absence of the hippocampal formation do not show any
VI
lack of the capacities attributed to the hippocampus. If the function
attributed to the hippocampus presupposes its unique morphological
organization and connections, one can wonder how this peculiar func
tion could be replaced by brain structures with completely different
organization and connections.
These serious uncertainties are sufficient for me to accept the pursuit
suggested by the titles of the present symposium as a new and promis
ing strategy. It seems reasonable and compelling to get closer to elemen
tary hippocampal processes by putting aside our preconceptions sug
gested by existing theories. This approach is also justified by the spec
tacular developments of electrophysiological, biochemical, and biophysi
cal techniques. It is, however, conceivable that investigations with these
highly refined techniques will uncover basic and universal processes of
neural plasticity rather than information on hippocampal functions. In
this context, because of its relatively simple organization, the hippocam
pus is undoubtedly one of the most promising targets among brain
structures. Insights gained concerning the basic processes of plasticity
would be a formidable achievement even if they do not add anything
special to understanding the function of the hippocampus itself. We
cannot however exclude the possibility that investigations with these
advanced methods might also uncover hippocampal mechanisms allow
ing the formulation of an entirely new hypothesis about its function
which has remained hidden so far just because of our traditional precon
ceptions.
Pecs, August 13, 1987 Endre Grastyan
Preface
This volume contains the papers presented at a satellite symposium on
synaptic plasticity in the hippocampus, held at Pecs, Hungary, on 13-15
August, 1987, preceding the International Brain Research Organisation
(IBRO) Congress in Budapest. The emblem of this symposium, as
depicted on the cover of this volume, was the triton, a winged hippocam
pus, the wings signifying plasticity.
The meeting was dedicated to Graham Goddard, who had agreed to
participate before his untimely death in a hiking accident in New Zealand
on 15 January 1987. T.V.P. Bliss gave an account on his life and person
ality.
Like the meeting, this book provides a comprehensive survey of the
rapidly growing field of hippocampal plasticity. The last decade has
generated a multitude of studies using in vitro model systems to examine
long-lasting changes at the synaptic level. At the same time, consider
able concern continues to be expressed regarding the significance of in
vitro findings for in vivo adaptive and maladaptive changes, such as
memory and epilepsy. Problems in interpreting the results of different
approaches and methods in the study of synaptic plasticity in the hip
pocampus were discussed by researchers from various disciplines: mor
phology, biochemistry, neurology, psychology, pharmacology, elec
trophysiology and molecular biology. Accordingly, the book is divided
into seven parts, focussing on problems of synaptic, transmitter, and
molecular mechanisms of long-term potentiation (LTP); control of hip
pocampal excitability, kindling and epilepsy; the LTP model; and phys
iological plasticity.
We are indebted to the Fonds fOr versuchstierfreie Forschung,
Zurich; Boehringer, Ingelheim, ER.G.; Upjohn, U.S.A.; Smith Kline &
French, U.K., and several local Hungarian firms whose sponsorship made
the symposium possible. Special thanks are extended to Gisela Gunther,
Mainz, and Zsuzsa Herzfeld, Pecs, who provided invaluable help with the
preparation of the meeting and the volume.
January, 1988 Helmut L. Haas, Mainz
Gyorgy Buzsaki, San Diego
Table of Contents
Foreword
E. GRASTYAN . v
Preface
H. L. HAAS and G. BuzsAKI VII
Synaptic Mechanisms of Long-Term Potentiation
Long-Term Potentiation of Feed-Forward Inhibition in the
Hippocampus: Extracellular Evidence
G. V. GODDARD, E. W. KAIRISS, W. C. ABRAHAM, and D. K. BILKEY . 3
Frequency Potentiation and Habituation in Hippocampal Area CA1
U. HEINEMANN, B. HAMON, R S. G. JONES, G. KOEHR, J. D. C. LAMBERT,
G. RAUSCHE, and P. SCHUBERT ..................... 6
Changes in Synaptic Transmission Evoked in the "In Vitro"
Hippocampal Slice by a Brief Decrease of [Mg++]o: A Correlate for
Long-Term Potentiation?
M. AVOLl, C. DRAPEAU, and G. KOSTOPOULOS . . . . . . . . . . . . . . 9
Postsynaptic Mechanisms in the Potentiation of Synaptic
Responses
K. L. ZBICZ and F. F. WEIGHT . . . . . . . . . . . . . . . . . . 13
Postsynaptic Mechanisms May Regulate Synaptic Strength by
Controlling Synapse Lifetimes
R MALINOW and H. T. CLINE . . . . . . . . . . . . . . . . . . . . . 17
Long-Term Potentiation of Inhibitory Responses in the Dentate
Gyrus
RJ. RACINE, M. deJoNGE, and T. KENNEDY . . . . . . . . . . . 21
Quantal Analysis of Synaptic Plasticity in the Hippocampus
C. YAMAMOTO, M. HIGASHIMA, and S. SAWADA . . . . . . . . . . . . . .. 24
x
Quantal Analysis of Long-Term Potentiation
L. L. VORONIN ................ . 27
Plasticity-Related Synaptic Mechanisms in Hippocampus
G. L. COLLINGRIDGE, C. E. HERRON, and RA.J. LESTER .... 31
NMDA Receptor Control of Spontaneous Complex Spike Discharge
in Hippocampal Pyramidal Cells
W. C. ABRAHAM and E. W. KAIRISS . . . . . . . . . . . . . . . . . . " 35
Mecamylamine Blocks Responses to NMDA and a Component of
Synaptic Transmission in Rat Hippocampal Slices
J. F. BLAKE, M. W. BROWN, N. AL-ANI, E.J. COAN, and G. L. COLLINGRIDGE . 38
LTP in the Recurrent Inhibitory Circuit of the Dentate Gyrus
M. L. ERRINGTON, H. L. HAAS, and T. V. P. BLIss . . . . . . . . . . . .. 42
NMDA Receptors May Be Involved in Generation of Hippocampal
Theta Rhythm
Z. HORVATH, A. KAMONDI, J. CZOPF, T. V. P. BLISS, and G. BuzsAKI .. " 45
Cytoplasmic Ca2+ Changes in Reference to Long-Term Potentiation
in the Hippocampal Slice
H. KATO, K. ITO, H. MIYAKAWA, A. OGURA, and Y. KUDo. . . . . . . . . .. 46
Electron Histochemical Localization of Calcium in CA1 of
Hippocampal Slices Following High-Frequency Stimulation: Effects
of Excitatory Amino Acid Antagonists
L. SIKLOS, U. KUHNT, F. Joo, and A. MIHALY. . . . . . . . . . . . . . .. 49
Transmitter Mechanisms of Long-Term Potentiation
Involvement of Serotonin in Hippocampal Plasticity
M. SEGAL and G. RICHTER ............... . 55
Norepinephrine Enhances Long-Term Potentiation at Hippocampal
Mossy Fiber Synapses
D. JOHNSTON, H. F. HOPKINS, and R GRAY . . . . . . . . . . . . . . . 57
Potentiation of Synaptic Transmission by Phorbol Esters Is
Accompanied by a Reduction of Physiological Adenosine Action
P. SCHUBERT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
An APV-Resistant Non-associative Form of Long-Term Potentiation
in the Rat Hippocampus
J.A. KAUER and RA. NICOLL . . . . . . . . . . . . . . . . . . . . .. 65
GABA Transmission in the Hippocampus: Postsynaptic Regulation
A. STELZER and R K. S. WONG. . . . . . . . . . . . . . . . . . . . .. 67
XI
Glycine Allosterically Regulates an NMDA Receptor Coupled Ion
Channel in Rat Hippocampal Membranes
D. W. BONHAUS, B. C. BURGE, and J. O. McNAMARA . . . . . . 70
MK-801 Prevents the Induction of Long-Term Potentiation
E.J. COAN, W. SAYWOOO, and G. L. COLLINGRIDGE . . . . . . . 73
Long-Term Potentiation in Slices from Human Hippocampus
H. L. HAAS, R. W. GREENE, B. HEIMRICH, and X. XIE . . . . . . . . 77
Decrease of GABA During Long-Term Potentiation in the CA1
Region of Rat Hippocampal Slices: Immunohistochemical and
Biochemical Analysis
Y. HORIKAWA, H. OKAMURA, I. HIROTSU, T. ISHIHARA, T. HASHIMOTO,
K. KURIYAMA, H. KIMURA, and Y. IBATA . . . . . . . . . . . . . . . . 81
What Does Long-Term Potentiation Model?
Synaptic Organization of Identified Neurons in the Hippocampus
M. FROTSCHER . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
Hippocampal Sharp Waves: A Physiological Correlate of LTP?
G. BuzsAKI and H. L. HAAS ................. 90
Characteristics of Associative Potentiation/Depression
W. B. LEW and N. L. DESMOND .............. . 93
Primed Burst Potentiation: Lasting Synaptic Plasticity Invoked by
Physiologically Patterned Stimulation
G. M. ROSE, D. M. DIAMOND, K. PANG, and T. V. DUNWIDDIE ....... 96
Collective Behaviors of the Hippocampal Slice-Epileptic and Non
epileptic
R. D. TRAUB, R. MILES, and R. K. S. WONG . . . . . . . . . . . . 99
Are Nerve Growth Factors Involved in Long-Term Synaptic
Potentiation in the Hippocampus and Spatial Memory?
B. R. SASTRY, S. S. CHIRWA, P. B. Y. MAY, H. MARETIC, G. PILLAI,
E.Y.H. KAO, and S.D. SIDHU ....................... 102
XII
Molecular Mechanisms of Long-Term Potentiation
Intracellular Injection of Protein Kinase C Causes Changes Similar
to Long-Term Potentiation
G.-Y. Hu, 0. HVALBY, S.1. WALAAS, K. ALBERT, P. GREENGARD, and
P. ANDERSEN . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109
On the Mechanism of Increased Transmitter Release in LTP:
Measurement of Calcium Concentration and Phosphatidylinositol
Turnover in CA3 Synaptosomes
M.A. LYNCH, M.P. CLEMENTS, M.L. ERRINGTON, and T.y'P. BLIss.. . 110
Effects of Phorbol Esters on Membrane Currents and Synaptic
Efficacy in the Hippocampus
D. V. MADISON, R. C. MALENKA, and R. A. NICOLL ....... 114
Gangliosides and Synaptic Plasticity in the Hippocampus
W, SEIFERT, A. WIERASZKO, and H. TERLAU. . . . . . . . . . . . . . .. 116
Long-Term Synaptic Potentiation and Macromolecular Changes in
Memory Formation
H. MATTHIES ................................ 119
Inhibitors of Protein Synthesis, but not mRNA Synthesis, Promote
Decay of Long-Term Potentiation in Rat Dentate Gyrus
S. OTANI, G.Y. GODDARD, C.J. MARSHALL, w'P. TATE, and w'C. ABRAHAM. 122
A Multi-Phase Model of Synaptic Long-Term Potentiation in
Hippocampal CA1 Neurones: Protein Kinase C Activation and
Protein Synthesis Are Required for the Maintenance of the Trace
K. REYMANN, U. FREY, and H. MATTHIES . . . . . . . . . . . . . . .. . 126
Modulation of Spike Repolarization in Hippocampal Neurones by
Tumor-Promoting Phorbol Esters
J. F. STORM ................................ 130
Control of Excitability in Hippocampus
Long-Term Potentiation in Relation to Kindling of the Rat
Hippocampus
F.H. LOPES DA SILVA, w,J. WADMAN, W, KAMPHUIS, B.P.C. MELCHERS, and
J. P. M. PIJN . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
The Role of M1 and M2 Receptors in Slow Muscarinic Excitation of
Hippocampal Neurons
U. MISGELD and W, MOLLER . . . . . . . . . . . . . . . . . . . . . . . . 137
