Presynaptic Receptors in the Mammalian Brain

208 Pages·1993·5.222 MB·English

by  Kenneth P. Scholz (auth.), Thomas V. Dunwiddie, David M. Lovinger (eds.)

Presynaptic Receptors
in the Mammalian Brain
Presynaptic Receptors
in the Mammalian Brain
Thomas V. Dunwiddie
David M. Lovinger
Editors
Birkhauser
Boston • Basel • Berlin
Thomas V. Dunwiddie
V.A. Medical Center and
University of Colorado Health Sciences Center
Department of Pharmacology C-236
Denver, CO 80220
USA
David M. Lovinger
Department of Molecular Physiology and Biophysics
Vanderbilt University School of Medicine
Nashville, TN 37232
USA
Library of Congress Cataloging-in-Publication Data
Presynaptic receptors in the mammalian brain / Thomas V. Dunwiddie,
David M. Lovinger, editors.
p. cm.
Includes bibliographical references and index.
1. Presynaptic receptors. I. Dunwiddie, Thomas V., 1951-
II. Lovinger, David M. (David Michael), 1959-
QP364.7.P72 1993 93-9565
599.0188-dc20 CIP
Printed on acid-free paper. Birkhauser
© 1993 Birkhliuser Boston
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ISBN-13: 978-1-4684-6827-4 e-ISBN-13: 978-1-4684-6825-0
DOl: 10.1 007/978-1-4684-6825-0
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987 654 3 2 1
Contents
Preface ...................................................... VB
List of Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. IX
1. Introductory Perspective
Kenneth P. Scholz .......................................... .
2. GABA Receptor-Mediated Inhibition of Synaptic Transmission in
B
the Hippocampus: Pharmacology and Intracellular Mechanisms
Patrick Dutar and Roger A. Nicoll. . . . . . . . . . . . . . . . . . . . . . . . . . .. 14
3. Muscarinic Cholinergic Inhibition of Glutamatergic Transmission
Stephen H. Williams and Daniel Johnston. . . . . . . . . . . . . . . . . . . . .. 27
4. Presynaptic and Postsynaptic Actions of Somatostatin in Area CAl
and the Dentate Gyrus of Rat and Rabbit Hippocampal Slices
Helen E. Scharfman . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 42
5. Presynaptic Actions of Opioids
Steven W. Johnson and R. Alan North. . . . . . . . . . . . . . . . . . . . . . . .. 71
6. Presynaptic Inhibition Mediated by Neuropeptide Y in the
Mammalian CNS: Possible Physiological Implications
William F. Colmers, A. Rory McQuiston, Samuel B. Kombian,
and Gloria J. Klapstein . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 87
7. Adenosine Modulation of Glutamate-Mediated Synaptic
Transmission in the Hippocampus
Carl R. Lupica and Thomas V. Dunwiddie. . . . . . . . . . . . . . . . . . . .. 104
8. Glutamate Autoreceptors in Mammalian Brain
David M. Lovinger and Nevin A. Lambert. . . . . . . . . . . . . . . . . . . .. 127
9. GABA Receptors on Inhibitory Neurons in the Hippocampus
B
Nevin A. Lambert and Neil L. Harrison. . . . . . . . . . . . . . . . . . . . . .. 143
VI Contents
10. The Role of Presynaptic GABA Receptors in Stimulus-Dependent
B
Disinhibition and the Induction of Long-Term Potentiation
Darrell V. Lewis, David D. Mott, H. Scott Swartzwelder, and
Cui-Wei Xie . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 161
11. Presynaptic Receptors and Quantal Models of Synaptic Transmission
John Clements. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 180
Keyword Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 197
Preface
Trying to address the entire field of presynaptic modulation of neurotransmitter
release is a rather daunting undertaking, one that is well beyond the scope of this
book. In addition, studies of release modulation, particularly from a biochemical
standpoint, have been the subjects of several extensive reviews, meetings, and
books (Langer, 1978; Chesselet, 1984; Wessler, 1989; Kalsner and Westfall,
1990), which provide an essential introduction to this subject. What we have
focused on, however, are several specific aspects of release modulation that
perhaps have not been as extensively discussed. First, we felt that it was important
to focus on modulation in the central nervous system; much of the work that has
been done in the past has emphasized the peripheral nervous system (e.g., the
autonomic nervous system and the neuromuscular junction), in part because such
preparations are more amenable to study. However, it is becoming clear that
modulation of release is, if anything, more important in the central nervous system
than in the periphery, and that virtually every transmitter system that has been
studied shows some type of release modulation.
The other way in which we have restricted the scope of this volume has been to
try to emphasize studies in which functional (primarily electrophysiological)
measures of transmitter release have been used rather than direct biochemical
measures of release, and to explore the ways in which release modulation affects
the normal physiological function at synapses. This emphasis on electrophysio
logical approaches has necessarily shifted the focus of these studies, and in some
cases has given unique insights into the importance of release modulation in neural
function. For example, it is now clear that modulation of transmitter release can be
quite important in higher order neural processes, such as the initiation oflong-term
potentiation (see Chapter 10). In addition, although there are difficulties with
using the postsynaptic cell as essentially an electrophysiological "transducer" to
measure transmitter release, this approach has numerous advantages as well. For
example, using electrophysiological measures of modulation permits a high
degree of temporal resolution that is not possible with conventional biochemical
approaches. Using electrophysiological techniques, we have been able to demon
strate that endogenously released adenosine and GABA modulate excitatory
transmission in the hippocampus on a very rapid time scale, with the maximal
inhibition of glutamate release occurring 250 ms after a stimulus, and recovery from
inhibition occurring within 1 s (Mitchell, Lupica, and Dunwiddie, unpublished). This
type of transient modulation of release could never be demonstrated biochemically,
because direct measurements of transmitter release usually lack both the sensitivity
and the time resolution required to demonstrate such transitory effects.
viii Preface
The electrophysiological approach to this issue has numerous other advantages
as well. For example, the involvement of presynaptic K+ and Ca2+ channels in
modulation can be examined more directly, and in many cases the specific channel
type that is affected by a neuromodulator can be identified by its physiological
characteristics. Quantal analysis of transmitter release at single synapses also has
the potential (although currently unexplored) of providing entirely different kinds
of insights into modulation. For example, two modulators might act on the same
synapse in different ways (e. g., one by changing the number of release sites, and
the other by changing the probability of release from a fixed number of sites) to
inhibit transmitter release; from a biochemical standpoint their effects would be
indistinguishable, while electrophysiological studies could demonstrate such
differences in their modes of action. This is not to say that electrophysiological
approaches have any inherent advantages over biochemical ones, but rather that
they each provide somewhat different kinds of information. Ideally, the two
approaches should be complementary, and when they can be simultaneously used
in the same system, they are particularly powerful.
On a final note, it is simply not possible to cover adequately even the
electrophysiological approaches to modulation, and we must apologize to the
groups who have examined modulation in a number of elegant systems that do not
even appear in this volume. The extensive studies of release modulation in
catecholamine systems in the central nervous system, and of modulation of release
from neurohypophysial terminals, are but two examples of such neglected
systems. The introductory chapter by Scholz does consider a number of other
biological systems not covered explicitly in the other chapters, and helps to
provide some additional perspective for these studies, but is by no means
exhaustive. Rather than be encyclopedic, we have chosen to restrict our focus to
some relatively closely related systems, some even involving the same synapse but
focusing on different modulators, in the hope that an in-depth analysis of a few
systems might prove more informative than a broader summary of the field.
Finally, in terms of future directions for research in this area, the existence of
neuromodulation seems to be well established in many systems, and we are at least
beginning to understand the mechanisms involved as well. The functional
relevance of neuromodulation has in most instances been much more difficult to
establish, but will no doubt be a major focus of future studies.
REFERENCES
Chesselet MF (1984): Presynaptic regulation of neurotransmitter release in the brain: facts
and hypothesis. Neuroscience 12:347-375
Kalsner S, Westfall TC, eds. (1990): Presynaptic Receptors and the Question ofA utoreg
ulation of Neurotransmitter Release. New York: New York Academy of Sciences
Langer SZ (1978): Presynaptic receptors and neurotransmission. Med Bioi 56:288-291
Wessler I (1989): Control of transmitter release from the motor nerve by presynaptic
nicotinic and muscarinic autoreceptors. Trends Pharmacol Sci. 10: llO-114
List of Contributors
John Clements, Vollum Institute, L474, Oregon Health Sciences University,
Portland, Oregon 97201, USA
William F. Colmers, Department of Pharmacology, University of Alberta, 9-36
MSB, Edmonton, Alberta CANADA T6G 2H7
Thomas V. Dunwiddie, Department of Pharmacology, C-236, University of
Colorado Health Sciences Center, 4200 East 9th Avenue, Denver, Colorado
80262, USA and Veterans Administration Medical Center 151, 1055 Cler
mont Street, Denver, Colorado 80220, USA
Patrick Dutar, Laboratoire de Physiopharmacologie du Systeme Nerveux,
INSERM U 161, 2 rue d' Alesia, 75014 Paris FRANCE
Neil L. Harrison, Department of Anesthesia and Critical Care, The University of
Chicago, Chicago, Illinois 60637, USA
Steven W. Johnson, Vollum Institute, Department of Neurology, Oregon Health
Sciences University, Portland, Oregon 97201, USA
Daniel Johnston, Division of Neuroscience, Baylor College of Medicine,
Houston, Texas 77030, USA
Gloria J. Kiapstein, Department of Pharmacology, University of Alberta, 9-36
MSB, Edmonton, Alberta CANADA T6G 2H7
Samuel B. Kombian, Department of Pharmacology, University of Alberta, 9-36
MSB, Edmonton, Alberta CANADA T6G 2H7
Nevin A. Lambert, Laboratory for Neurological Research, V A Medical Center,
Duke University, 508 Fulton Street, Durham, North Carolina 27705, USA
Darrell V. Lewis, Department of Pediatrics, Duke University Medical Center,
Box 3430, Durham, North Carolina 27710, USA
x List of Contributors
David M. Lovinger, Department of Molecular Physiology and Biophysics,
Vanderbilt University School of Medicine, Nashville, Tennessee 37232,
USA
Carl R. Lupica, Department of Pharmacology, C-236, University of Colorado
Health Sciences Center, 4200 East 9th Avenue, Denver, Colorado 80220,
USA
A. Rory McQuiston, Department of Pharmacology, University of Alberta, 9-36
MSB, Edmonton, Alberta CANADA T6G 2H7
David D. Mott, Department of Pediatrics, Duke University Medical Center,
Durham, North Carolina 27710, USA
Roger A. Nicoll, School of Medicine, Department of Pharmacology, University
of California, San Francisco, California 94143, USA
R. Alan North, Vollum Institute, Department of Neurology, Oregon Health
Sciences University, Portland, Oregon 97201, USA
Helen E. Scharfman, Neurology Research Center, Helen Hayes Hospital, West
Haverstraw, New York 10993-1195, USA
Kenneth P. Scholz, Dept. of Pharmacological & Physiological Sciences, Univer
sity of Chicago, 947 East 58th Street, Chicago, Illinois 60637, USA
H. Scott Swartzwelder, Department of Psychiatry, Duke University Medical
Center, Durham, North Carolina 27710, USA
Stephen H. Williams, Division of Neuroscience, Baylor College of Medicine,
Houston, Texas 77030, USA
Cui-Wei Xie, Department of Pediatrics, Duke University Medical Center,
Durham, North Carolina 27710, USA
CHAPTER 1
Introductory Perspective
KENNETH P. SCHOLZ
Two purposes guided the writing of this introductory chapter. My fIrst objective
was to provide a concise history and background to the topic covered in this book.
In doing so, I have drawn from specific examples of presynaptic inhibition that are
not addressed in later chapters. This is an attempt to bind together work performed
on a variety of preparations to provide an expanded view of our understanding of
the mechanisms of presynaptic inhibition and how this understanding was
obtained. It is anticipated that a discussion of these issues will expose important
links between mechanisms of presynaptic inhibition in different preparations. A
more thorough historical background can be obtained from Eccles (1964) and
Nicoll and Alger (1979). My second objective was to present areas of research that
I believe will be important in the near future or that perhaps deserve more attention
than they have received.
Presynaptic inhibition is studied with a number of different approaches. These
could be classifIed roughly into two categories: electrophysiological approaches
and biochemical approaches. This chapter and book focus primarily on the study
of presynaptic inhibition by electrophysiological techniques, with the results from
biochemical experiments borne in mind. Those interested in studies of presynaptic
inhibition that utilize biochemical approaches are referred to Kalsner and Westfall
(1990) as a good starting point.
HISTORICAL OVERVIEW
Presynaptic Inhibition in Monosynaptic Reflex Circuits and at Crayfish
Neuromuscular Junction
As pointed out by Eccles (1964), reflex inhibition of muscle contraction was
perhaps the first example of presynaptic inhibition. Liddell and Sherrington (1925)
and Cooper and Creed (1927) showed that contraction of a muscle triggered
inhibition of tonus in the antagonistic muscle. This was initially attributed to
postsynaptic inhibitory mechanisms acting on the motor neurons in the spinal cord
(Brock et al., 1952). However, it was laterrecognized by Frank and Fuortes (1957;
Presynaptic Receptors in the Mammalian Brain
Thomas v. Dunwiddie and David M. Lovinger, Editors
© 1993 Birkhiiuser Boston